Advances in Botanical Research, Volume 16

Advances in

BOTANICAL RESEARCH VOLUME 16

Advances in

BOTANICAL RESEARCH Editor-in-Chief J. A. CALLOW

Editorial Board H. W. WOOLHOUSE W. D. P. STEWART

W. G . CHALONER E. A. C. MAcROBBIE

Advances in

BOTANICAL RESEARCH Edited bji

J. A. CALLOW

VOLUME 16

I989

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CONTRIBUTORS TO VOLUME 16

P. R . BELL, Deparlment of' Botcmj~ant1 Microbiology, University College, London U'CIE 6B7: U K J. L. HARWOOD, Deprirtrnent of' Biochemistry, University College, Cardif CFI IXL, UK P. M . HOLLIGAN, Murirw Biologid Association qf the U K , Cituriel Hill, Pljwiouth PLI 2PB, U K A . L. JONES, Depcirtment of' Biochemistry, ~Jnirvrsity College, Curdif CFI I X L . U K R . A . SPICEK. Dt>purtment of' Earth Sciences, IJniversity of Oxford, Parks Roud, O.yfiwdOX1 3PR. U K

This Page Intentionally Left Blank

PREFACE

This volume of A h w i c r s in Botunicul RoscurcIi contains articles on lipid metabolism in algae (Harwood and Jones), the alternation of generations (Bell). the formation and interpretation of plant fossil assemblages (Spicer) and primary productivity in the shelf seas of N W Europe (Holligan). Lipid metabolism in algae is extremely diverse which is not unexpected given the diverse evolutionary origins of the group. The review by Harwood and Jones considers the broad range of lipid structures and underlying metabolic processes found in the algae, biit concentrates on results of the relatively few detailed studies that have been made in genera of microalgae such as C 1 1 / u t ~ ~ ~ ~ t i o tDuti(ilidlu, ~ i o t i ~ . ~ . Atiuc:l:vris. and some of the ‘higher’ marine algae such as the fucoids. The relative paucity of detailed studics on algae suggests that further study will be rewarding in uncovering novel pathways that could be important in biotcchnological exploitation. The phenomenon of ‘alternation of generations’, or the change in phase coincident with meiosis, used to form the backbone of elementary botanical training. Unfortunately. its association with often uninspired teaching based on ‘types’ has probably led botanists largely to neglect advanced study of this basic and radical shift in plant development, and the scientific opportunities afforded by lower plants in which this change of phase can be most clearly observed. This situation may change as molecular biologists seek good ‘systems’ in which to study changes in gene-expression and associated triggers or signals. Certainly the morphological events associated with the haplophase/diplophase transition are amenable to analysis by the exciting new molecular technologies and, especially for those without training in classical botany, the article by Bell is a good, thought-provoking introduction to the whole subject of alternation of generations, its basic characteristics in a whole range of plant groups, the associated ultrastructural changes, and an outline of the very small amount of experimental work that has been done so far. ‘Taphonomy’ is the study of the processes of fossilization and is therefore of fundamental importance to the accurate interpretation of the fossil record, and the reconstruction of ancient communities and environments. It is a subject that is relatively new and requires highly integrated multidisciplinary approaches for most effective study. In his substantial review, Spicer considers the various types of fossilization process, and there is a particularly vii

...

Vlll

PREFACE

fascinating account of how recent volcanic eruptions, and especially the events of Mount Saint Helens in 1980, have provided excellent opportunities to observe the consequences of explosive vulcanism in shaping one aspect of the fossil record. The stability of the global environment is currently a ‘hot topic’ in science and accurate predictions of the dynamics of populations, relevant, for example, to the proper exploitation of biological resources and the control of environmental degradation, requires reliable estimates of the various processes leading to the exchange of materials in different components of the global ecosystem. In the final chapter of this volume, Holligan reviews understanding of the ecology and productivity of the important phytoplankton component of marine systems, specifically in the shelf seas of NW Europe. While much is known of the temporal and spatial aspects of phytoplankton growth and the physiological and environmental factors controlling it, less appears to be known about aspects of productivity and the flux of materials through phytoplankton. Holligan considers how improved methodologies and greater cognisance of the physical mixing process in tidally-stirred shelf seas will improve our understanding of productivity. Finally I would like to thank all the authors of articles in this volume for their patience with the editor and their efforts to make his task easier. J. A . CALLOW

CONTENTS

CONTRIBUTORS T O VOLUME 16. . . . . . . . . . .

V

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vii

PREFACE.

Lipid Metabolism in Algae JOHN L. HARWOOD and A. LESLEY JONES I. 11. 111.

Introduction .

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1

Lipid Structures .

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2

Lipid Composition of Algae . . . . . . . . . . . . . . A. Fatty Acids . . . . . . . . . . . . . . . . . . B. Lipid Classes . . . . . . . . . . . . . . . . .

5 5 9

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12

V . Metabolism of Lipids in Cyanobacteria (Blue-Green Algae)

. . .

13

Studies with Halotolerant and Halophilic Dunulirllu Species

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19

Metabolism in Marine Algae . . . . . . . . . . . . . . A. Labelling Characteristics . . . . . . . . . . . . . B. Positional Distribution ofAlgal Fatty Acids . . . . . . . C. EKccts of the Environment on Algal Lipid Metabolism. . . .

28 28 33

VIII. Lipid Metabolism in Other Algal Types . . . . . . . . . .

42

IV. General Remarks on Plant Lipid Metabolism

VI.

VII.

IX.

Conclusions

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35

47

The Alternation of Generations PETER R. BELL I.

Introduction . . . . . . . . . . . . . . . . . . .

11. The Universality of Life Cycles .

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ix

55 56

CONTENTS

X

I11 . Essential Features of Points of Change . . . . . . . . . . A . Gametogenesis . . . . . . . . . . . . . . . . . B. Sporogenesis . . . . . . . . . . . . . . . . .

57 57 65

IV . The Significant Features of Aberrant Cycles . . . . . . . . . A . Aberrant Cycles in Natural Conditions . . . . . . . . . B . Induced Aberrations in Sexual Cycles . . . . . . . . .

70 70 72

V . The Causal Approach to Alternation . . . A . General Assumptions . . . . . . B . From Gametophyte to Sporophyte in the C . From Sporophyte to Gametophyte . . VI . General Conclusion .

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. . . . . . . . Lower Plants . . . . . . . . . . .

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78 78 78 82 87

The Formation and Interpretation of Plant Fossil Assemblages ROBERT A . SPICER 1.

Introduction . . . . . . . . . . . . . . . . . . . A . The Quality of the Plant Fossil Record . . . . . . . . . B. Vegetational Heterogeneity . . . . . . . . . . . . .

96 98 100

I1 . Plant Remains as Sedimentary Particles . . . . . . . . . . A . Allochthonous and Autochthonous Assemblages . . . . . B . Settling Velocity . . . . . . . . . . . . . . . .

101 101

111. Aerial Dispersal andTransport ofplant Organs . . . . . . . A . Leaf Abscission . . . . . . . . . . . . . . . .

104 104 106

B.

Organ Dispersal by Wind

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103

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112

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114 115 119 122

VI . Fluvial Transport . . . . . . . . . . . . . . . . . A . Channel Deposits . . . . . . . . . . . . . . . .

125 126

VII . Lacustrine Environments . . . . . . . . . . . . . . . A . Fluvio-lacustrine Deltas . . . . . . . . . . . . . .

130 133

IV .

Litter Degradation o n the Forest Floor

V . Aquatic Processing of Plant Debris . A . Initial Processes-Floating . . B . Transport in the Water Column C . Lcaf Degradation . . . . .

VIII . Fluvio-marine Deltas and Estuaries . A . Pro-delta Slope . . . . . . B . Distributary Mouth Bars . . C . Tidal Flats . . . . . . . D . Interdistributary Embayments .

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140 141 142 143 144

xi

CONTENTS

E . Beaches . . . . . . . . . . . . . F . Lower Delta Plain Marshes . . . . . . . G . Upper Delta Plain Marshes . . . . . . . H . Deltaic Lacustrine and Fluvial Environments. I . Detrital I'cats . . . . . . . . . . .

IX .

Peat and Coal Assemblages

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147

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X . Vulcanism . . . . . . . . . . . . . . . . . . . A . The Importancc of Explosive Vulcanism to the Plant Fossil Record: Case Studies . . . . . . . . . . . . . B . Debris Flows . . . . . . . . . . . . . . . C . Preservation in Air-kill Tephra . . . . . . . . . 1) . Lateral Lakes in Volcanic Tcrrnins . . . . . . . . E . Post-eruption Vcgetation Recovery . . . . . . . . XI .

Prcservation and Diagcncsis . Conipt-cssion'lmpressions B . Duripartic Prcscrvation . C . Tissue Mineralization . D . Casts and Moulds . . . A.

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151

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152 160 166

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168

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172 175 175 176 I76 178

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179 1x0 180 1x1

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183

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184

XI1 . Applications of Plant Taphonomy to the Fossil Record . . . A . Specimen Morphology and Taxonomy . . . . . . . B . C om m it ni t y Reco 11s t r uc t i on . . . . . . . . . . C . Rcconstructing Community Suites a n d Regional Vegetation D . The llse of Plant Fossils in Sedimentology . . . . . . XI I I . Conclusions

i44 145 146 147 147

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Primary Productivity in the Shelf Seas of North-West Europe P . M . HOLLIGAN I.

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194

I1 . Ecological and Physiological Perspectives . . . . . . . . . . A . Ph y t o pla n k to 11 Distributions . . . . . . . . . . . . B . Control of Phytoplankton Production . . . . . . . . .

196 196 202

Ill.

Introduction .

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Methods for Estimating Primary Productivity A . Nutrient Budgets . . . . . . . . B . Oxygen and Carbon Fluxes . . . . . C . Biomass Distributions . . . . . . D . Primary Productivity Models . . . .

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IV . Environmental Conditions for Phytoplankton Growth in the NW European Shelf Scas . . . . . . . . . . . . . . . A . Mixing, Processes, Seasonal Stratification . . . . . . . . B. Light Availability . . . . . . . . . . . . . . . .

212 212 213 215 217 217 217 220

Lipid Metabolism in Algae

JOHN L. HARWOOD and A . LESLEY JONES

Dtpwtmeiit of' Biochemistry, University College CurdiflL CardiffCF1 I X L , U K

I. 11.

Introduction .

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.

Lipid Composition o f Algae. . . . . A. FattyAcids. . . . . . . . . B. Lipid Classes . . . . . . . .

IV.

General Remarks on Plant Lipid Metabolism .

v1.

VII.

VIII. IX.

i

2

Lipid Structures

Ill.

V.

. . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

5 5 9

. .

12

. .

13

Studies with Halotolerant and Halophilic Dunuliellu Species . . . .

19

Metabolism in Marine Algae . . . . . . . . . . . . . A. Labelling Characteristics . . . . . . . . . . . . . B. Positional Distribution of Algal Fatty Acids . . . . . . . C. Effects of the Environment on Algal Lipid Metabolism . . .

. . . .

28 28 33 35

. . . . . .

42

. . . . . . . . . . . . . . . . .

47

Metabolism of Lipids in Cyanobacteria (Blue-Green Algae) . .

Lipid Metabolism in Other Algal Types . . . . . Conclusions .

.

. I.

INTRODUCTION

Algae are an extremely diverse group of organisms. Not surprisingly, thereAdvances in Botanical Research Vol. 16 ISBN 0-12-005916-9

Copyright $2 1989 Academic Press Limited All rights of reproduction on any form reserved.

2

J O H N L. H A R W O O D A N D A . LESLEY J O N E S

fore. their lipid composition and metabolism are exceptionally varied. In this chapter we have concentrated attention on groups of organisms which have been studied in reasonable detail. This selection has, in consequence, neglected some interesting, but isolated, studies. Nevertheless, we believe that it allows readers unfaniiliar with lipids to assimilate more useful information. I n any case. plenty of reviews dealing with specialized aspects are referenced. In order to lay a basis for further discussion of metabolism, we have begun with sections on lipid structure and occurrence in algae. The metabolic sections then deal with organisms of increasing complexity. from the primitive cyanobacteria to marine macroalgae. Finally. we end with a section devoted mainly to green algae, which can be regarded as the nearest in metabolic characteristics to higher plants.

11.

LIPID STRUCTURES

The complex lipids of plants are mainly amphiphilic molecules with a hydrophobic head group and a hydrophilic “tail”, enabling them to form the lipid bilayers of membranes. Algae contain many of the lipids found in higher plants, and also some unusual lipids. The basic structure is a glycerol backbone derived from glycerol 3-phosphate (from the photosynthetic Calvin cycle, or glycolysis) to which is esterified the hydrophobic head group. Phospholipids have phosphate esterified to the sn-3 position with further moieties esterified through this. Glycolipids have sugar moieties as a head group. The structures of the major phospholipids and glycolipids found in algae are given in Fig. 1. Most of the eukaryotic algae contain a range of phospholipids and glycolipids, many of which are found in higher plants. However, the prokaryotic cyanobacteria have only the lipids of the chloroplast thylakoids of higher plants: namely monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), sulphoquinovosyldiacylglycerol (SQDG) and phosphatidylglycerol (PG) (Fig. 2) (Gounaris e f al., 1986). Tri- and tetragalactosyldiacylglycerols have been found in some higher plants, and Chlorrllu contains trigalactosylglycerol (Benson e f al., 1958). Sugars other than galactose may be found. Some red algae have mannose and rhamnose in their glycolipids (Pettitt, T. R., Jones, A. L. and Harwood, J. L., unpublished). Monoglucosyldiaglycerol (MGlcDG) was found in Nostoe calcicnla (Feige et al., 1980) and Anuhaena variahilis (Sato and Murata, 1982a). In A . variuhilis, MGlcDG appeared to be a metabolic intermediate, being rapidly converted to MGDG by epimerization of C-4 of glucose (Section V). Pham-Quang and Laur (1976a,b,c) found a range of novel glycolipids, phospholipids and sulpholipids in three brown algae, Pelvetia canuliculufn, Fucus vesiculosus and F. serratus. The two Fucus spp. also contain one major

3

LIPID METABOLISM IN ALGAE

unknown lipid (Smith and Harwood, 1984a; Jones and Harwood, 1987). In C. c r i s p s and P. lunosa, 3SS-labellingrevealed a number of sulphur-containing lipids, most of which were minor components (Pettitt, T. R.. Jones, A. L. and Harwood, J. L., unpublished). However. one of these lipids was identified as phosphatidylsulphocholine (PSC), the sulphonium analogue of phosphatidylcholine (PC) (Fig. 3). which has also been identified in diatoms and a Euglena species (Anderson ct ul., 1978a,b; Bisseret L ’ t d.,1984).

ALlprd

X

PA

-H

PC

-Ct$CH2N(CH3)3

PE

+ -C H2C $N H3

PS

+ 4H2CHNHj

+

I

cooOH

OH

PI

PG

DPG

-CH

C$OC-R

I

I

I

0Fig. I . Structures of common phosphoglycerides. PC, phosphatidylcholine; PI, phosphatidylinositol; PE, phosphatidylethanolamine; PG, phosphatidylglycerol; PA, phosphatidic acid. Based on Harwood and Russell (1984).

4

JOHN L. HARWOOD A N D A. LESLEY JONES

Chlorosulpholipids have also been found in some algae and are a major component of Ochromonas danica (Elovson and Vagelos, 1969). An unusual lipid found in a number of green algae and some lower plants, but not detected in angiosperms, is the homoserine ether lipid 1(3),2-diacylglyceryl-(3)-O-4'-(N,N,N-trimethyl)-homoserine (DGTS) (Fig. 4), first identified in 0. danica (Brown and Elovson, 1974). This lipid has since been

X -

Lipid

MGDG

DGDG

?H

I

SQ DG

CH20H

C H2-S Fig. 2 . Structures of common glycosylglycerides.

4-

LIPID METABOLISM IN ALGAE

5

0Fig. 3 . Structure of the sulphonium analoguc ofphosphatidylcholinc

Fig. 4. Diacylglycerol trimethylhomoserine ether lipid. identified in Chlumydomonus reinhurdtii, Dunuliellu sulina, Codium spp., Ulvu pertusu and Enteromorphu intestinalis (Sato and Furuya, 1984a,b), and is a major lipid of Chlumydomonus reinhurcitii and D. sulinu (Eichenberger, 1982; Norman and Thompson, l985b). Algae also contain neutral lipids, mostly as triacylglycerols which are, presumably, storage products (Pohl and Zurheide, 1979a,b) with small amounts of mono- and diacylglycerols. They also contain various hydrocarbons as minor constituents and a range of sterols and sterol esters (see Pohl and Zurheide, 1979a). Thus the range of lipid structures in algae varies from the simple constituents of the cyanobacteria to the complex variety in the eukaryotic brown (and other) algae. The structures found vary between the algal divisions and some lipids appear to be characteristic of different algal divisions-for instance, DGTS is found in many Chlorophyceae but has never been detected in any Phaeophyceae. The distribution of lipids within different algae is considered in more detail in the following section.

111.

LIPID COMPOSITION OF ALGAE A. FATTY ACIDS

A large number of algae have now been analysed for their fatty acyl composition. The convenience and sensitivity of gas-liquid chromatographic

6

J O H N L. H A R W O O D A N D A . LESLEY JONES

(GLC) methods have made this possible, whereas, in contrast. there has been much less work on the content of individual lipid classes in either marine or fresh-water algae. Fresh-water algae typically contain similar fatty acids to terrestrial plants. However, the proportions of such acids differ considerably from, for example, higher plant leaves. In general, even-chain acids in the range C,,C,, account for the bulk of the components. In contrast to plant leaves, fresh-water algae usually have a relatively high proportion of C , , fatty acids and reduced levels of C, unsaturatcd fatty acids, especially r-linolenate (Harwood rt d.. 1989). Of course, the total fatty acid composition of organisms gives little information about the specific acyl contents of individual complex lipids, which are usually very different. For example, it has been noted by several authors that triacylglycerols that can accumulate in certain species of algae are usually very low in polyunsaturated fatty acids (e.g. Tornabene ('I u/.. 1983). in contrast to total algal extracts (see Hitchcock and Nichols, 1971). Furthermore, in an analysis of the individual lipids of two strains of Chlam?.doomotiu.F rc.inhardtii. Eichenberger et ul. (1986) noted that. whereas the glycosylglycerides. PG and phosphatidylinositol (PI) contain mainly or exclusively the n-3 isomer of linolenic acid, phosphatidylethanolamine (PE) and DGTS contained the 11-6isomer (1'-linolenate). I n addition, it should be remembered that environmental factors such as light, temperature, nitrogen levels. salt stress or pollution can have a marked effect on fatty acid (and lipid) composition. Representative fatty acid compositions of some fresh-water and salttolerant algae are given in Table I. It will be seen that whereas the C, fatty acids are absent (or only found in trace amounts) in fresh-water algae, these acids may be significant components of organisms living in high-salt environments such as the Dead Sea. In fact, for marine algae the very long chain polyunsaturated fatty acids arachidonic acid and eicosapentaenoic acid (n-3) are usually major components (Pohl and Zurheide. 1979a; Harwood r t al., 1989). Marine algae in general contain a bewildering array of major fatty acids. Some representative examples of compositions for phytoplankton and macroalgae are shown in Table TI. Palmitate is, invariably, the major saturated fatty acid of phytoplankton with myristate often being found in appreciable quantities. In contrast to higher plants, C,, fatty acids are less important, with palmitoleic acid being the major monoenoic acid component. In some cases, e.g. Monochrysis lathrri (Table 11), total C,, acids represent a very minor proportion of the total acyl constituents. One common theme for all marine algae, with the exception of the Chlorophyceae, is that C, polyenoic acids are major constituents. Arachidonic and eicosapentaenoic ( n - 3 ) acids are the main C,, acids and sometimes represent a very high proportion of the total acyl groups of particular lipids. For example, in F. serratus arachidonate accounted for 67% of PC (Smith and

7

L I P I D M E T A B O L I S M IN A L G A E

F a t t y acid composition (“A, total)

16:O 16: I 16:2 l h : 3 16:4 18: I 18:2 I X : 3 1X:4 3 0 : s 3 2 : h F r e s h w a t c r spp.

Scene~1rsniu.sohliquus 35 Clik>r~llti vulguris 26 Chumy1onionu.s 20 reitiliurdt ii S a l t - t o l e r a n t spp. Anki.st,otli~.sriiusspp. I.socI1r:v.vis spp. Nuiinoclrliwi.r spp.

13

3 8 4

tr.

tr.

15

7

2

-

9 2

1

4

23

7

1

14 15 -

25

I

3

12 6 9 2 0

~

~~

7

9

4 4

6 34 6

30 20

2

30

3

2 6 1

29 17

2

~

I - -

1

2 27

-

13 ~~

Data from Hitchcock and Nichols (19711, Hen-Amotz and Tornabene (198.5) and Eichenberger el t i / . (1986). Fatty acids are abbreviated with the figure before the colciii indicatinp tlic number of carbon atoms. and the figure alter the colon indicating the number of double bonds contained.

Harwood, 1984a). while in Chondrus crispus eicosapentaenoate represented more than 25% of the total acids of the glycosylglycerides (Pettitt c ~ tul., 1989). The unicellular marine alga Chnrtonclla untiyuu (Raphidophyccac) was also found to contain rather higher amounts of eicosapentaenoate in all lipid classes (Sato er a/., 1987). A very unusual fatty acid which is found in photosynthetic tissues From higher plants is truns-A3-hexadecenoate. This acid is locatcd exclusively at the sn-2 position of PG (Harwood, 1980a). Interestingly. in view of the postulates concerning its possible role in granal stacking (see Bolton et d., 1978). the same acid is also found in PG in algae with quite different chloroplast morphology. Thus, it has been reported in brown algae (Smith and Harwood, 1983), red algae (Pettitt and Harwood, 1986), Raphidophyceae (Sato et a/., 1987) and diatoms (Kawaguchi er al., 1987). Together with all the negative evidence from higher plants (Bolton er d.,1978), it is clear that whatever the role truns-A3-hexadecenoate plays in nature, it is not in granal stacking. More likely explanations concern its possible involvement with chlorophyll-protein complexes (Remy er al. 1982), as suggested by modelbuilding experiments (Foley and Harwood, 1982; see Foley er ul., 1988). Cyanobacteria, as an evolutionarily less advanced “algal” group, also contain much more simple lipid and fatty acid compositions than other algae. Murata and Nishida (1987) have divided cyanobacteria into four groups based on the original classifications of Kenyon et al. (1972). Examples of each of these four groups are shown in Table I l l . Strains in the first group contain only saturated and mono-unsaturated fatty acids, while those in the other three groups contain linoleate plus polyunsaturated acids characteristic

Fatty acid composition ( "/o total) 14:O 16:O 16:1

Phytoplankton Monochrysis lutheri (Chrysophyccac) Olisthodiscus spp. (Xanthophyceae) Lauderiu borealis (Bacillariophyceae) Amphiciinium carterue (Dinophyceae) Dunaliellu sulinu (Chlorophyceae) Hemiselmis hrutiescens (Cryptophyceac) Macroalgae Fucus vesiculosus (Phaeophyceae) Chondrus crispus (Rhodophyceae) U l w luctuca (Chlorophyccae) Fatty acid abbreviations as for Table I

10 X

16:2

13 14

22 10

5 2

16:3 16:4 7 2 12 tr.

18:l

I I

3 4

4

7

12

21

3

3 tr.

24

1

41

--

-

1

13

IS 3

1 tr.

3

tr.

tr.

2

tr.

26

-

21 34

1

18

-

2 6 2

tr. tr. tr.

~

-

1

1 ~

-

18

18:2

2 5 11

9 9

I t 6 1 1 8 tr.

18:3

18:4

2 8

r .

1 tr. 2 1 1 9

20:4 20:s 1

~~

5 -

1

8

2 1 9 1 3 -

-

9

30

tr.

10 1

7

4

IS

1

4

18

2

17

24

I

14 14

8 22 2

22:6 7 2

25 -

-

tr.

9

LIPID METABOLISM IN ALGAE

Group

1

2 3 4

Fatty acid composition ('YO total)

Organism

Anrrcj~.stisnidu1rti.s Atiuhicctm vrrriuhilis Sjnechoiystis 67 14 To1jpotliri.u tenuis

46 32 28 22

46 22 4 3

3 I1 5 16

0 17 17 15

0 16

0 6

0 0 3i 13

0 0 0 II

Data taken from Murata and Nishida (19x7). where rel'crences will he found. €.'ally acid ahhrovations as for Table I .

of each group. Thus, groups 2, 3 and 4 contain a-linolenate, ;j-linolenate and octadecatetraenoate (n-3), respectively (Table I1 1). Filamentous blue-green algae are distributed throughout the four groups, while the prokaryotic green alga Prochloron has a fatty acyl composition placing i t in the first group (Kenrick er d., 1984). B.

LIPID CLASSES

Just as the cyanobacteria contain a relatively simple fatty acid composition, so is their lipid content confined to four major classes only-monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DCDG), sulphoquinovosyldiacylglycerol (SQDG) and phosphatidylglycerol (PG). A minor lipid, monoglucosyldiacylglycerol (MClcDG), accounts for a trace amount in some species such as Anucysris vuriahilis but not in others (e.g. Anucystik niduluns). This minor lipid is involved in the biosynthesis of MGDG (see later). The lipid compositions of two cyanobacteria and Prochloron spp. are given in Table IV. When individual membrane fractions were isolated from Anacystis niduluns, the thylakoid, plasma and outer membrane all contained a rather similar amount of the four lipids except that DGDG was somewhat enriched in the outer membrane. However, the lipid content as a percentage of the dry weight was very different, being 57%, 19% and 3% for the plasma, thylakoid and outer membranes, respectively (Murata and Nishida, 1987). In nitrogen-fixing cyanobacteria unusual glycolipids have been reported. These are found i n the heterocysts of the filamentous heterocystous strains as well as in unicellular strains. In A . cylindricu, the glycolipids account for 4.4% of the total lipids. The chemical structures of the four main nonsaponifiable glycolipids were determined about 15 years ago (Bryce e t al., 1972; Lambein and Wolk, 1973) and other minor variants have been reported (see Murata and Nishida, 1987). Eukaryotic algae contain a formidable range of acyl lipids. As a general-

I0

J O H N L. H A R W O O D A N D A. LESLEY JONES

Lipid (YOtotal)

Organism

..IIItrhrrefltr L'oric/hi/i.s

nitluluti.s Proc~/l/ororlspp. A n i i ~ ' j . .tis \

MGDG

MGlcDG

DGDG

SQDG

PG

54 57

I 1i.m.

17 11 II

II II 26

21 5

_5 T_

3

17

not measured. Data takcn from Muratu a n d Nishida ( 19x7). where the original references can be found.

ii.ni. =

ization, the three glycosylglycerides (MGDG, D G D G and SQDG) are major constituents. So far as phosphoglycerides are concerned. all the main classes can usually be detected. Insufficient data are available for generalizations to be made but it appears, thus far, that there are considerable differences between algal divisions in their relative contents of individual phospholipids. Some examples of lipid compositions are given in Table V. DGTS is an unusual lipid which is found in the Chlorophyta, although it was first reported in the chromophyte 0. (lunicu (Nichols and Appleby, 1969; Brown and Elovson, 1974). I t represents a major component in green algae such as Ch1rini~~tlot~iotiu.v rrinhurcltii (Eichenberger and Boschetti, 1978; Table V). and a survey of its occurrence in non-vascular green plants has been made (Sato and Furuya, 1985). Apart from 0. dunicu, Chuttonrllu untiyuu (Sato r t ul., 1987: Table V) is the only chromophyte known to contain DGTS. The lipid has not been reported in brown algae (e.g. Smith and Harwood, 1984a) or diatoms (e.g. Kawaguchi P / ul., 1987). Many fresh-water algae contain chlorosulpholipids (Mercer and Davies, 1979). Again, it was work with 0. dunicu which first revealed large amounts of these lipids (Haines and Block, 1962). The substances were soon identified as sulphur esters that were present in amounts greater than for most glycolipids or phospholipids in the cell. Many of the sulphur esters also contain chlorine, and are therefore known as chlorosulpholipids. In 0. dunicu they represent about 15% of the total lipids. They have been detected in all freshwater species but not in any of the marine species examined (Mercer and Davies, 1979).These unusual lipids have been reviewed (Haines, 1973a,b). Certain diatoms have been found to contain other novel sulphur-containing lipids (Kates, 1987). Characteristically, all species examined contain three sulpholipids in addition to SQDG. They have been identified in Nitzchiu ulhu as sterol sulphate, deoxyceramide sulphonic acid and the PC analogue PSC (Anderson rt ul., 1978a,b; Kates rt ul., 1978). In the non-photosynthetic diatom N. albu, PSC completely replaced PC, but in other diatoms both lipids occurrcd together (Kates, 1987). Overall, the sulpholipids are major constituents of diatoms, representing 30Y0 of the total polar lipids in N. pelliculnsu

TABLE V Tlw acjl lipid conipositiotis Lipid ( O h ) PC PE PI PG DPG Other phospholipids MGDG

DGDG SQDG Other glycolipids DGTS Lipid X Neutral lipids Free fatty acids

Chatronella antiqud

Dutiuliella parvu

Aceiahulnriu meditarraticw ‘

9 n.d. 2 6

0.1 I .2 0.6 3

__

29 18 29 ~

6

of .sonic

ulgue

Chlat?i~.clot?ioti~i.s reiniiurdiiid

31 20 20

3

10

4.2’ 6.2 2.9

.-

37

A_-

5.4 ~

41 16 7

16.9 14.8 15.5

15.0 11.3 22.0

16

n.d.

n.d. 24. I 4.9

-

~

20

Fucus wsicuIosusJ

30.1 1 .5 trace 1.1 1.9

5

~

21 11 7 1 15

CIlOt1dr us crispus ‘’

-

~

3.4 2.2

I5 13

“Sato et ul. (1987); bKates (1987); ‘Eichenberger and Gerber (1987); dEichenberger et ul. (1986); ‘Pettitt n.d. = not detected.

el

ul. (1988b); ’Unpublished data

12

JOHN L. HARWOOD AND A. LESLEY JONES

and over 74% in N . alba. PSC has also been detected in marine red algae such as Chondrus crispus and Polysiphonia lanosa (Pettitt et al., 1988b). A review of the lipids of marine algae has been made by Pohl and Zurheide (1979a). There have been sporadic reports of a wide range of unusual structures. However, in many cases these have not been confirmed and may, in at least some cases, be the products of lipid degradation or modification during analysis. Such processes are well known in plant tissues, and special precautions must be taken to prevent their occurrence (see Harwood, 1980a).

IV. GENERAL REMARKS ON PLANT LIPID METABOLISM A detailed discussion of plant lipid synthesis is beyond the scope of this chapter, and, moreover, specific algal aspects will be dealt with later. However, a few very general remarks together with comprehensive references will be made here. Fatty acid metabolism has been reviewed very recently (Harwood, 1988). De novo synthesis involves the concerted action of acetyl-CoA carboxylase and a type I1 (dissociable) fatty acid synthetase. The end-product of such synthesis is palmitoyl-ACP, which can be specifically chain-lengthened to stearoyl-ACP using a special condensing enzyme. Thus C,, and C,, saturated fatty acids are the products of de novo synthesis. The first unsaturated bond is usually introduced at the A9-position by a desaturase which probably uses acyl-ACP substrates in most instances. Palmitoleic and oleic acids result from this action. Further desaturations are thought to involve complex lipid substrates such as PC and MGDG (Harwood, 1988). These may take place within choroplasts (prokaryotic pathways) or include extra-chloroplastic (eukaryotic pathway) enzymes. Fatty acids can also be elongated, and such reactions are clearly of great importance to many algae where C,, fatty acids are major constituents. Nothing is known about the substrates for such reactions in algae, although acyl-CoAs are used in a number of higher plant tissues (Harwood, 1988). Obviously, where both chain elongation and desaturation are involved in the formation of a given fatty acid, there will be more than one possible route. Thus, arachidonate has been shown in some algae to be formed by a desaturation-elongation-desaturation route from linoleate (Nichols and Appleby, 1969): 18 : 2 (n-6)+18 : 3 (n-6)+20 : 3 (n-6)+20 : 4 (n-6) In contrast, in a euglenoid (Hulanicka et al., 1964) it appears to be formed thus: 18 : 2 (n-6)+20 : 2 (n-6)+20 : 3 (n-6)+20 :4 (n-6)

LIPID METABOLISM IN ALGAE

13

So far as complex lipids are concerned, the formation of MGDG and DGDG (Joyard and Douce, 1987), SQDG (Harwood, 1980b; Mudd and Kleppinger-Sparace, 1987) and phospholipids (Moore, 1982; Harwood 1989) has been reviewed. The metabolism of unusual lipids such as the sulpholipids of diatoms (see Kates, 1987). chlorosulpholipids (Mercer et d.,1374) and DGTS (see Schlapfer and Eichenberger, 1983) has also been discussed. In addition, the arsenic lipid (arsenoribosylphosphatidylglycerol) which appears to mediate arsenic excretion in marine organisms has been discussed (Benson, 1987). Other general aspects of plant lipid metabolism will be found in the excellent volumes edited by Stumpf (Stumpf and Conn, 1980, 1987).

V.

METABOLISM OF LIPIDS IN CYANOBACTERIA (BLUE- GREEN ALGAE)

The cyanobacteria, like the eukaryotic algae, have an oxygen-evolving photosynthetic mechanism, yet their prokaryotic morphology makes study of their metabolism much simpler. Their lipid composition and metabolism have been recently covered in an excellent review (Murata and Nishida, 1987), so only a few aspects will be dealt with here. The plasma and thylakoid membranes of cyanobacteria contain glycerolipids-almost exclusively MGDG, DGDG, SQDG and PG. The outer membrane contains lipopolysaccharides and hydrocarbons in addition to glycerolipids. In addition, some nitrogen-fixing species of filamentous cyanobacteria may contain vegetative cells which change into heterocysts (Haselkorn, 1978). These heterocysts contain a refractile multilayered heterocyst envelope which contains unique glycolipids (glycosidic glycolipids and glycosyl ester glycolipids) (Lambein and Wolk, 1973). The glycerolipid composition of several species of cyanobacteria is shown in Table IV. It is noteworthy that the only glycerolipids present in appreciable amounts are those which are regarded traditionally as typical chloroplast thylakoid lipids (Harwood, 1980a; Gounaris rt d.,1986). In addition, it will be seen that for Anucysfis nzduluns, where more detailed analyses have been undertaken, the lipid compositions of different membranes in the cyanobacterium are broadly similar. However, the lipid contents (YO dry weight) are quite different, being 19%, 57% and 3% for the thykaloid, plasma and outer membranes, respectively (Murata and Nishida, 1987). In addition to the four main lipid classes present in cyanobacterial membranes, MGlcDG seems to be a ubiquitous, though minor, component (Feige, 1978). When the fatty acids of cyanobacterial lipids were first studied, it was realized that although these were broadly similar to those of higher plant chloroplasts, there were some notable differences. These include the increased

14

JOHN L. HARWOOD AND A. LESLEY JONES

,

importance of C (especially palmitoleic) acids, the relative reduced prevalence of polyunsaturated fatty acids (including the absence of linoleate and alinolenate from some organisms), the presence of y-linolenate in some cyanobacteria and an absence of trans-A3-hexadecenoate from PG (Hitchcock and Nichols, 1971; Murata and Nishida, 1987). Some efforts have been made to classify cyanobacteria into four subgroups, according to their fatty acyl composition (Kenyon, 1972; Kenyon et al., 1972) (see Section 111). Examples of fatty acid compositions for different organisms are given in Table 111. The individual glycerolipids differ from one another in their acyl compositions. In general, MGDG and DGDG contain the highest ratios of unsaturated to saturated acids. In those cyanobacteria which contain polyunsaturated fatty acids, the latter are also enriched in the glycosylglycerides. The two acidic glycerolipids, SQDG and PG, tend to contain very large amounts of palmitate with only small quantities of palmitoleate. Naturally, the fatty acyl compositions of cyanobacteria and their glycerolipids are very dependent on growth temperature (see later). All glycerolipids of cyanobacteria display the typical "prokaryotic" positional concentration of C,, acids at the sn-1 position and C , , acids at the sn-2 position (Zepke et al., 1978). Studies using ['"C] acetate first established the rapid labelling of all major glycerolipid classes (Nichols, 1968). When H14C0, was used for pulselabelling of 30 species of cyanobacteria, the first lipid highly labelled was MGlcDG. Later, radioactivity appeared in MGDG, and it was proposed that these lipids had a precursor-product relationship (Feige et al., 1980). Moreover, analysis of the glucose and galactose moieties of these two lipids in Anacystis nidulans showed a similar relationship (Fig. 5) and indicated that the sugar moiety was not lost during this interconversion. As a result of these experiments, Sat0 and Murata (l982a) proposed that the mechanism of formation of MGDG involved epimerization at the C-4 atom of the precursor glucose unit. In addition, experiments with cerulenin (see below) suggested that DGDG was formed by galactosylation of MGDG rather than via a glycolipid : glycolipid transferase (see Joyard and Douce, 1987). Cerulenin, a known inhibitor of fatty acid biosynthesis, was tested with Anacystis nidulans. Its inclusion reduced severely the incorporation of radioactivity from H1"C03 into all lipid classes except D GDG (Sato and Murata, 1982a). This was in keeping with the idea that newly synthesized acyl chains are needed for the overall formation of glycerolipids, but because DGDG can be synthesized by galactosylation of MGDG, its labelling is less affected. Indeed, analysis of the sugar residues of D G D G confirmed that a high proportion of the total radioactivity of this lipid was present in the galactose moieties (Sato and Murata, 1982a). A membrane-bound UDP-glucose : diacylglycerol glucosyl transferase was detected in A . variubilis (Sato and Murata, 1982a). This enzyme seems to be present in both thylakoid and plasma membranes (Omata and Murata, 1986) and it is interesting that, in higher plants, the equivalent galactosyl

LIPID METABOLISM IN ALGAE

I

15

r

Time ( h ) after labelling

(a)

(b)

Fig. 5. Changes in the radioactivity of monoglucosyl- and monogalactosyldiacylglycerol during pulse-labelling from HI4CO, in A . niduluns and subsequent chase. Gal, galactose; Glc, glucose. Taken from Sato and Murata (1982a)with permission. transferase is found in the chloroplast envelope and, in some cases, also in prothylakoids (see Murata and Nishida, 1987). Fatty acid synthesis was followed in A . vuriubilis by labelling from H14C03 (Sato and Murata, 1982b). Radioactivity was incorporated initially into palmitate, stearate and oleate. In fact, it was suggested that saturated fatty acids were initially incorporated into complex lipids such as MGlcDG and that subsequent desaturations occurred while the acyl groups remained attached to complex lipids. This was in agreement with proposals for higher plants (see Harwood, 1988). Examination of molecular species labelling of individual lipid classes led to proposals that in MGlcDG, stearate could be desaturated to oleate and linoleate but hardly at all to linolenate. In contrast, MGDG was an efficient substrate for successive desaturation of stearate through to linolenate as well as for that of palmitate to hexadecadienoate. DGDG did not appear to be used for desaturation, whereas successive desaturation of stearate, but not of palmitate, appeared to occur on PG and SQDG (Fig. 6). Direct demonstration of lipid-linked desaturation of palmitate in MGDG was made by the use of isotopic labelling. Incubation of cells with H13C03 caused the formation of MGDG enriched in its acyl groups. After 2.5 h, 19% of the palmitate but virtually none of the palmitoleate at the sn-2 positions were enriched in 13C. During a subsequent incubation for 7.5 h in the presence of unlabelled CO, and the fatty acid synthesis inhibitor cerulenin,

16

JOHN L. HARWOOD A N D A. LESLEY JONES

38°C

22°C

18:O 16:O [Gal

1

1

18:l 16:l [Gal

--+

E

18:2

GalDG

--+

18:l 16:O [Gal

- -1

18:3 16:O

18:Z

18:3 16:l

18:2

16:O

[Gal

L

[g;: -[

1611 Gal

Gal

1

Gal

18:3 16:2 Gal

I

1

1

I

I

J

Fig. 6. Pathways for the desaturation of fatty acids esterified to the acyl lipids of A . niduluns. Taken from Sato and Murata (1982b) with permission.

[I3C]palmitate was desaturated to [13C]palmitoleate.Mass spectrometric analysis of the 2-acylglycerol moiety showed that [L3C]palmitoyl[ I 3C]glycerol was converted to [ 3C]palmitoleoyl-['3C]glycerol, and ['ZC]palmitoyl-['zC]glycerol to ['ZC]palmitoleoyl-['ZC]glycerol. If a pathway involving deacylation, desaturation and reacylation had been involved, then this would have been expected to yield products containing partial enrichment (Fig. 7) and this was not found. The results were fully in support of an MGDG-linked desaturation of palmitate (Sato et al., 1986). The idea that desaturation of fatty acids in cyanobacteria required lipidlinked substrates was in agreement with data for A . variahilis reported by Lem and Stumpf (1984a). They showed that cell-free extracts were able to synthesize palmitate and stearate but not oleate from [14C]malonyl-CoA.In addition, although [14C]palmitoyl-ACPcould be elongated to ['4C]stearoylACP, n o desaturation was detected. When ['4C]stearoyl-ACP was used as

LIPID METABOLISM IN ALGAE

17

Lipid- linked desaturation

Gly ( U 1-16; 0 ( U) Gly (E)-16:0 ( E l

Gly(U )-16 : 1(U 1 Deacylat ion desaturation and reacylatton

Gly( E 1-16 : 1 ( U )

Fig. 7. Principle of isotopic species analysis to discriminate between the two possible mechanisms of dcsaturation of palmitate. Combinations of the glycerol backbone and the C16 acids at the sn-2 positions of MGDG are presented as Gly-16:O and Gly-16:I. U, unenriched; E. enriched with I T . Redrawn from Sato rt ul. (1986) with permission.

substrate in a A9-desaturase assay, activity was detected in green algae such as C. pyrenoidom, Scenedesmus ohliquus and Chlamydomonas moewensii, but not in A . variahilis or Nostoc spp. Data from other laboratories agree with the above conclusions (Stapleton and Jaworski, 1984b; Al Araji and Walton, 1980). The fatty acid synthetase of A . variahilis is of the type I1 non-associated type (see Harwood, 1988). The malonyl-CoA : ACP transacylase has been purified and found to have rather similar properties to that from spinach chloroplasts (Stapleton and Jaworski, 1984a). The elongation of palmitate to stearate uses palmitoyl-ACP and NADPH and not palmitoyl-CoA or NADH (Lem and Stumpf, 1984a; Stapleton and Jaworski, 1984a). Radioactivity from ['4C]acyl-ACPs was rapidly transferred into complex lipids, especially MGDG, by crude cell extracts of A . variahilis. The first intermediate detected was diacylglycerol (Lem and Stumpf, 1984b), but one presumes that the incorporation into this compound was due to glycerol 3-phosphate acylation and phosphatidate phosphatase. Acyl-CoAs could not act as substrates. Although [14C]oleoyl-ACPwas effective for acylation, the probable lack of formation of this compound in vivo (see above) would prevent the esterification of this moiety which would have to be formed by lipid-linked desaturation (Sato and Murata, 1982b). Compositional studies on cyanobacteria have demonstrated that shifts in growth temperature lead to several types of changes in lipids. In Anacystis

18

JOHN 1.. HARWOOD A N D A . LESLEY JONES

TABLE VI Chunge~in the moleculur .species composition qf’glycerolipids 0f’Anabaena variabilis c u u s t d by growth ietnperuture Lipid

Growth temp. ( C)

Molecular species (YOtotal) C-l C-2

GlcDG MGDG

DGDG PG

SQDG

38 22

18.0 1 8 . 1 1 8 . 2 1 8 : 3 1 8 . 1 1 8 : 2 1 8 . 3 1 8 . 3 1 6 . 0 1 6 . 0 1 6 . 0 16:O 16.1 16.1 1 6 . 1 1 6 . 2

24 22

60 40

10 24

38

1

25

22

2

2

23 12

38 22

1 1

16 4

24 20

0 19

1

56 10

41 26

48 10

26 16

sx

38

...77

0

38 22

10

2

0 6

0 0

0 0

0 0

0 0

1

11

34

0

35 3

0 32

0 12

16 I

38

0 0 3 1 4

0 61

0 0

0 0

0 0

0 0

0

0 0

0 0

0 0

0 0

9

Fatty acid abbreviations as in Table I . Taken from Murata (1987). with perinission

niciuluns, lowering growth temperature led to an increase in unsaturation and a shortening of chain length (Holton et a/., 1964). Similar changes were found with S~~nec.hococcu.s cedrorum (Sherman, 1979), and in S. lividus lowtemperature growth led to a decrease in palmitate and oleate and an increase of palmitoleate in MGDG and DGDG while stearate decreased and palmitoleate and oleate increased in PG and SQDG (Fork et ul., 1979). In Anucjxtis nidulrms, lowering growth temperature led to a decrease in chain length of mono-unsaturated acids at the sn-I position of all lipids but increased desaturation of palmitate at the sn-2 position of MGDG and D GDG (Sato et d., 1979). In contrast to the above, the unicellular cyanobacterium A . variahilis contains polyunsaturated fatty acids. Lowered growth temperatures led to an increase in a-linolenate at the sn-l position of all lipids, while the composition of C, acids at the sn-2 position remained nearly constant apart from a slight increase in hexadecadienoate in MGDG and DGD G (Sato et al., 1979; Sat0 and Murata, I980b). These experiments are summarized in Table VT, where the molecular species patterns for different lipid classes are shown. In temperature-shift experiments it has been found that A . variahilis rapidly alters its fatty acid composition as well as the positional distribution of such acids on individual glycerolipids. For example, for 10 h after a change in growth temperature from 38 ’C to 28 ‘C, the total amounts of lipids

LIP113 METABOLISM IN ALGAE

19

stayed constant but a desaturation of palmitate at the . ~ n - 2position of M G D G took place (Sato and Murata, 1980a). Molccular oxygen was required for the desaturation, which was prevented by chloraniphenicol or rifanipicin, suggesting that the specific A9-desaturase activity was induced by the downward shift in temperature (Sato and Murata, 1981). Slower decreases in the amounts of oleate and linoleate and commensurate increases in 3-linolenate which occur in M G D G and SQDG and PG were also prevented by protein synthesis o r R N A synthesis inhibitors (Sato and Murata. 1981). Conversely, sudden increases in growth temperature transiently increase de novo fatty acid synthesis but suppress desaturation of existing lipids in A . vuriuhilis (Sato and Murata, 1980a). The rapid changes in unsaturation levels of C , , acids only occurred in M G D G , in keeping with its role in palmitate desaturation (above). Slower changes in the unsaturation of C , fatty acids occurred in all major lipid classes (Murata, 1987). The changes which were found in the lipids of cyanobacterial membranes have been related to an adaptive response to prcvcnt damage caused by low temperatures. The results have been fully discussed (Murata. 1987: MuraLa and Nishida, 1987). I t appears that the plasma membrane (rather than the thylakoids) is particularly susceptible to low-temperature stress in both A nucysl is n iduluns and A nuhuenu vur iuhilis. Apart from temperature, a number of other environmental factors have been shown to alter lipid composition in cyanobacteria. These eKects are summarized in Table V11. Mention was made of the unusual heterocyst glycolipids a t the beginning of this section. These compounds have the structures shown in Fig. 8. The biosynthesis of these glycolipids was first studied by [I4C]acetate incorporation (Abreu-Grobois c t d . ,1977). I t was suggested that hydroxylation of the aliphatic chain at the C-3 and C-25 positions took place after the fatty alcohol was linked to the glycosides. Krespki and Walton ( 1 983) compared the formation of heterocyst glycolipids and glycerolipids during heterocyst formation. They concluded that biosynthesis of the hydrocarbon moieties of heterocyst glycolipids was regulated independently of fatty acid synthesis. In addition, they suggested that a n enzyme system for the hydroxylation of aliphatic hydrocarbon chains of the glycolipids was activated transiently during heterocyst formation. This process and heterocyst glycolipid synthesis are both increased by 7-azatryptophan (Krepski and Walton, 1983). Mohy-UdDhin el ul. (1982) suggested that the latter increased one or more steps of primary alkanol synthesis, making the (2-25 hydroxylation rate-limiting for the formation of the glycoside containing 1,3,-hexacosanetriol.

VI. STUDIES WITH HALOTOLERANT AND HALOPHILIC D U N A L I E L L A SPECIES Dunuliclla spp. possess some special features which make them attractive ex-

20

Environmental change

JOHN L. HARWOOD A N D A. LESLEY JONES

Organism

Effect

Reference

Nitrate increase ilnciej~s1i.rnidu1un.s .Spirul/nu pltrtc~I1.si.s Microc,j,stisuerugiiioscr 0.5cillur oriu ru hrscens

16:01 I 6 : I f 18:2t 18:31 N o change N o change

Piorreck ei nl. (1984) Piorreck P I a/. (1984) Piorreck ei ul. ( 1 984) Piorreck P I uI. ( 1984)

Increasing culture age

Agnienrlluni yuurlruplicuruni Anuh~rrnrrwriuhilis

16: 1. 18: It 1 8 : 2 , Olsonandingram 18:3J ( 1975) 18: l t 1 6 : O . 1 8 : 2 1 Gusevrru/.(1980)

Anaerobic growth

Apli~tio~lirc~c~ hulophj~ticu18 : 21 O.sc,iNtrtoriu linineticu No change

Oren ei a / . ( 1985)

Light presence

Various

No change

Kenyon el ul. ( 1972)

Light intensity

Anuc.j.sti.7 riidulnns

16:0, 1 8 : I f 1 6 : I J DohlerandDatz with increased light (1980)

Light quality

Anrrc~j~sti.~ nit1ulnn.s

GI ycerolipid changes

Temperature drop

Various

Chain length1 Unsaturationt See text Molecular species changes

Datz and Dohler (1981)

Fatty acid abbreviations as in Table I

perimental models. They grow rapidly under axenic conditions to yield populations of very homogeneous cells. Since they are without cell walls, they are easily disrupted and can therefore be separated into relatively pure subcellular fractions. Their lipid composition is rather similar to that of higher plants and is typical of green algae. Moreover, their ability to tolerate a wide range of temperatures and salinities (Brown and Borowitzka, 1979) allows the effects of these environmental stresses on metabolism to be studied. The lipids of two halotolerant species of Dunuliellu, ( D . purva and D.terriolectu) (Evons et ul., 1982a) and six halophilic species (D.viridis from the Dead Sea and various unidentified species from the Sinai) (Evans and Kates, 1984) have been examined. All these species were found to contain high proportions (40 mol %) of glycosylglycerides and low proportions (20 mol YO) of phosphoglycerides. The main glycolipids were MGDG, D G D G and SQDG. The main phospholipids were PG and PC. Analyses for the two halotolerant and two halophilic species are shown in Table VIII.

21

LIPID METABOLISM IN ALGAE

Glycosyl ester glycobpids

Glycosd~cglycolipi@

a-0-Glucopyranos yl 25-hydroxyhexacosa~te

3,2 5-Dihydroxyhexacosanyl-0-D-glycopyranoside

no

no

0- a n d

on

no ou

( 9 0 -1. )

0-D-Glucop yranosyl 25.27-dihydroxyoctacosaMte

Fig. 8.

OH

( 1 0 'I. )

YY

noon

on

3,25.27-Trihydroxyoctacosanyl-a-Dglycopyranoside

Structures of heterocyst glycolipids of cyanobacteria

TABLE VIII Lipid composit ion of h u b tolerant and haloph ilic Dun a I iella species Lipid

D. parva

Phosphatidylcholine Phosphatid ylethanolamine Phosphatidylinositol Phosphatid ylglycerol Phosphatidic acid Total phospholipid

9 n.d. 2 6 n.d 17

Monogalactosyldiacy lglycerol Digalactosyldiacylgl ycerol Sulphoquinovosyldiacylglycerol Other glycolipids Total glycolipids

21 II 7 I -

Diacylglycerol-0-(N,N,N-trimethyl)homoserine Non-esterified fatty acid Neutral lipids

D. tertiolecta

4 2 3

8 2 -

C,

D, ,

1 1 tr.

2 1 tr.

4 3 tr. n.d -

19

6

6

22 21

22 19

24

3

9

7 25

15 14 14 tr. tr. 55 53

40

10 tr. 53

15

8

13 15

7

14

15

21

Data expressed as mol YOand taken from Kates (1987) with permission n.d. = not detected.

22

J O H N L. H A R W O O D A N D A . LESLEY JONES

In general, halophilic species had lower levels of phospholipids and proportionally higher amounts of glycosylglycerides than halotolerant species. Moreover, PI, which was found in appreciable amounts in halotolerant species, was only found in trace amounts in the halophilic species. PE was not detected in D. parva. Significant amounts of neutral lipids, principally triacylglycerols and nonesterified fatty acids, were found in all species. These represented 15-25 mol YO and 7-14 niol ‘4, respectively, of the total lipid contents. Interestingly, diacylglycerol-O-4’-( N.N,N-trimethyl)-homoserine was identified as a major component (3 ~ 1 mol 4 Y O )in all species examined (Evans et al.. 1982b). As mentioned in Section 111, this zwitterionic non-phospholipid has been found in many algal species (Eichenberger, 1982; Sato and Furuya, 1985). including D. hrirckau~il(Fried Ct a/., 1982). I t is common also in lower plants (Sato and Furuya, 1984a,b) but has not been detected in any angiosperms or gymnosperms examined. The fatty acids of individual lipid fractions from all Dunalirlla species showed characteristics typical of other plant types, including angiosperms. Thus, palmitate was the major saturated fatty acid and this was enriched in SQDG of the glycolipids. The two galactosylglycerides were enriched in polyunsaturated fatty acids. MGDG was enriched in a-linoleic and hexadecatetraenoic acids. while DGDG contained high amounts of linoleic and x-linolenic acids. DGTS also contained a similar fatty acid content to DGDG. As in higher plants, PG contained high amounts of trans-A3hexadecenoate as well as appreciable amounts of palmitate, linoleate and alinolenate. D . .salina has been extensively studied at the subcellular level by Thompson’s group. Firstly, studies were made of phospholipid metabolism during growth at 30 C or 12 C or after temperature shifts. Generation times were found to correspond approximately to a Q,, of 2. with times of 20 h at 30 C and 80 h at 12 ‘C. Both cultures reached the same cell density but had rather different lipid and protein contents. In general, cells cultured at 12 C had a higher protein and acyl lipid content but a lower chlorophyll content than those grown at 30 C. Interestingly, the chlorophyll ujh ratio was 2.77 at 30 C but 4.09 at 12 C (Lynch and Thompson, 1982). The relative changes in acyl lipid and chlorophyll contents could be correlated with a proportional decrease in thylakoid membranes but an overall increase in cell volume at 12 C. When cells were shifted from 30°C to 12”C, no division occurred for about 96 h, after which division resumed, with a generation time of 80 h. The major particulate subcellular fractions were the chloroplast and microsomal. Whereas the chloroplast fraction was enriched at least four-fold in glycolipids compared to phospholipids, the microsomal fraction contained about twice as much phospholipid as glycolipid. Moreover, the relative proportion of cell phospholipid contained in chloroplasts was significantly reduced when cells were shifted to, or grown at, 12°C. This reflected the relat-

LIPID METABOLISM IN A L G A E

23

ive increase in microsomal menibrancs compared to thylakoids for cclls grown at lower temperatures (Lynch and Thompson, 1982). When the proportions of individual phospholipids of chloroplast or microsoma1 membranes were analysed, they were found to change little with growth temperature. For cells grown at either 30 C or 12 C, the major phospholipids of chloroplasts were PG and PC with smaller amounts of PE and PI. Microsomal menibranes contained PE and PC as the main phospholipids. In contrast, the relative proportions of glycolipids responded to temperature change. In particular, the relative content o f D G D G increased and that of M G D G decreased at 12 C. The ratio of M G D G to DGDG therefore changed from 3.4 in chloroplasts from 30 C cells to 2.1 for 12 C cells. Because poikilotherms need to maintain membrane fluidity at different growth temperatures, it was not surprising that phospholipid unsaturation was increased at 12 C for both chloroplast and microsomal membranes. In temperature-shift studies. the majority of these changes occurred after more than 60 h for chloroplast fatty acids. In the microsomal fraction, significant decreases in palmitate and increases in octadecatrienoate contents were seen within 12 h of temperature shift. Similarly, changes in the fatty acyl content of DGTS were also greater in the microsonial membranes. In contrast, the fatty acid patterns of the chloroplastic glycolipids changed little in response to growth temperature (Lynch and Thompson, 1982). The rather slow response of fatty acid unsaturation to shifts in growth temperature--especially for the chloroplast membranes-raised the obvious question as to how poikilotherms are able to withstand sudden changes in environmental conditions. Following observations with cyanobacteria (Section V), where an “emergency response” seemed to be the retailoring of individual molecular species (Sato and Murata, 198Oa,b), the phospholipids of D..sulinu membranes were examined in more detail. The individual phospholipids were isolated following thin-layer chromatography (TLC). a n d converted to diacylglycerols by digestion with phospholipase C; the diacylglycerols were separated by G L C of trimethylsilyl derivatives. Such procedures showed that there were significant changes in the molecular species of PE and PG. F o r PE there was a decrease in C,, species and co,ncomitant increases in C,, and C,, species. Changes associated with PG included the detection of a new molecular species, dioleoyl, not found at 30 C. Although there were some, limited, changes in fatty acid unsaturation detected during the first 12 h of low-temperature acclimation, it was concluded that the initial alterations in response to low temperatures involved discrete changes in certain molecular species. Such changes in molecular species composition would then augment the effects of acyl chain unsaturation in modifying membrane fluidity (Lynch and Thompson, 1984a). As mentioned above, changes in the fatty acyl composition of chloroplast phospholipids were much slower than for microsomal components. Thus only minor alterations in phospholipid acyl chain compositions were evident

24

JOHN L. HARWOOD A N D A. LESLEY JONES

after 36 h of shifting cells from 30 to 12 C. Between 36 h and 60 h, increases in the percentage of palmitate and a-linolenate were observed in PG. These alterations were accompanied by decreases in trans-A3-hexadecenoate and linoleate (Lynch and Thompson, 1984b). In contrast, the fatty acyl composi:ion of the other main chloroplast phospholipid, PC, did not alter very much over the 60-h period. Changes in the molecular species distribution for PC and PG were also seen after 60-h acclimation. The molecular species changes for PG correlated well with the overall fatty acyl changes. Thus, the 18 : 2/16 : I species was particularly reduced, in keeping with the decrease in both linoleate and rrans-A3hexadecenoate. Significant increases in molecular species containing palmitate and r-linolenate were seen-again in keeping with the fatty acid analysis (Lynch and Thompson. I984b). The change in molecular species of PG which occurred between 36 h and 60 h, following a shift in growth temperature, coincided with a large change in the threshold temperature of thermal desaturation of the photosynthetic apparatus. This was measured by chlorophyll fluorescence and, since lipid compositional changes other than those associated with PG were negligible during this period, suggested that a correlation existed between the molecular species of composition of PG and the thermal stability of the photosynthetic membrane. Taken together with the data on microsomal membrane compositional changes, the experiments suggested strongly that the initial steps in cellular acclimation to low temperatures involved molecular species retailoring. These changes then augmented the effects of increased acyl chain unsaturation as a means of restoring appropriate membrane properties (Lynch and Thompson, 1984~). Further studies on the subtle changes in acyl lipid molecular species used HPLC as the separation technique. Because of the poor absorbance of lipids in the UV. initial quantitation used the laborious procedure of effluent splitting and measurement by GLC of fatty acid methyl esters (Lynch and Thompson, 1983). However, the development of a flame ionization detector allowed more rapid quantitation and the procedure was applied to the analysis of D.sdina PG and galactosylglycerides (Smith et a/., 1985; Cho and Thompson, 1987). In Section IV, mention was made of the so-called prokaryotic and eukaryotic pathways for fatty acid and acyl lipid synthesis in eukaryotic organisms. The relationship between these two pathways in D.salznu was investigated in detail through radiolabelling with [I4C]palmitate, [I4C]oleate and [14C]laurateas precursors. Since only [I4C]laurate could be elongated in D. salina, palmitate gave rise to C,, acids only and oleate to C, , acids (Norman eta/., 1985). After a 2-min incubation with 4 pCi of [I-14C]palmitate, about 3% of the isotope was taken up per 5 x lo8 cells. This allowed experiments to be conducted with a 2-min labelling period followed by a chase period. During the total incubation a gradual movement of radioactivity was

LIPID METABOLISM IN ALGAE

25

seen from the microsomal membranes to the chloroplasts. This movement was associated with a decrease in phospholipid labelling and an increase in that of glycolipids. When the individual acyl groups were analysed, it was found that phospholipids only contained [I4C]palmitate. In contrast, glycolipids contained unsaturated C,, acids. After a 16-h chase, over 30% of the glycolipid radioactivity was accounted for by [14C]hexadecatetraenoate. Similarly, when [14C]oleatewas used in labelling studies, the radioactivity was incorporated initially into phospholipids of the microsomal membranes. After only a 20-min chase more than 50% of this microsomal phospholipid labelling was in the form of [*4C]linoleate,showing the presence of an active extra-chloroplastic A1 2-desaturase. By 16 h, chloroplast phospholipids contained 58% and 12% of their radioactivity in linoleate and sr-linolenate, respectively. In contrast, chloroplast glycolipids contained over 70% of their radioactivity as a-linolenate. These results confirmed that in D.salina, as in higher plants (Harwood, 1988), desaturation of oleate occurs mainly outside the chloroplasts, followed by transfer of the resultant linoleate back into plastids for its desaturation to a-linolenate in association with glycosylglycerides. When [I4C]lauratewas used as precursor, the acid entered the chloroplast quite rapidly, where it was used by the de n o w synthesizing enzymes and gave rise to radiolabelled C,, and C , , fatty acids. Moreover, in contrast to [ 14C]palmitate labelling, [‘4C]laurate incorporation resulted in the accumulation of appreciable [’4C]trans-A3-hexadecenoate. These studies were extended to a consideration of the molecular species of PG which were radiolabelled during temperature stress. When[14C]palmitate was used as precursor for a 2-min pulse, the specific radioactivity of PG was higher initially than that of any other microsomal phospholipid. The major molecular species of microsomal PG (80%) was 16 : 0/18 : 2, with about 45% of the 16 : O/ 16 : 0 species. Smaller amounts of 16 : O/ 14 : 2 species were also present (Lynch and Thompson, 1984a). In spite of the heavy concentration of 16 : 0 at the sn-l position, analysis of the radiolabelled PG by phospholipase A, digestion revealed that 30% of the [I4C]palmitate wgs present initially at the sn-2 position. In fact, immediately after labelling, the specific radioactivity of the palmitate at the sn-2 position was 10 times that at the sn- 1 position. Molecular species analysis by HPLC confirmed that [I4C]palmitate was preferentially incorporated into the 16 : 0/16 : 0 species. During the cold-chase period a changing pattern of incorporation of [L4C]palmitateinto either microsomal or chloroplast PG was seen. Thus, whereas microsomal PG always contained more radioactivity at the sn-l position, chloroplast PG initially contained radioactivity almost exclusively at the sn-2 position. With time, both positions of chloroplast PG became equally labelled. These results indicate the “prokaryotic” nature of chloroplast PG synthesis initially, and it is only later that molecular species of presumed microsomal origin appear in the plastid (Norman and Thompson,

26

J O H N L. HARWOOD A N D A. LESLEY JONES

I985a). I n fact, further analysis of the chloroplastic molecular species showed that 18: 2/16: 0 was labelled initially, followed only later by 16: Ojl8 : 2 species. When [I"C]laurate was used as precursor, the acid was rapidly taken up by chloroplasts, where it was used by fatty acid synthetase to produce [14C]palmitate and [14C]stearate, and the latter was desaturated to [14C]oleate.These products were rapidly exported to the endoplasmic reticulum, where PG was labelled more rapidly than other microsomal phospholipids. I n marked contrast, chloroplast PG contained no radiolabelled C , fatty acids. Immediately after the 2-min labelling period, this phospholipid contained large amounts of ['4C]laurate, but within 10 min of chase, [I"C]palmitate was the major radiolabelled moiety. In keeping with the proposal that 1 -acyl,2-palmitoyl-PG is the substrate for the A3-desaturase (Harwood and James, 1975), the decline in radioactive palmitate during the 20-60-min chase period was matched by an equivalent rise in the labelling of truns-A3-hexadecenoate. As mentioned above. the proportions of dilrerent cellular membranes in Dutitrlir//rr changes with low-temperature growth. There were also significant changes in the metabolism of chilled cells. Thus, for example. there was no delay in the labelling of the sn-l position of chloroplast PG from [lSC]palmitatein chilled cells. This was due to the increased contribution of "eukaryotic" (microsomal) metabolism at lower temperatures. Moreover, this was in keeping with the previous observations that the molecular species composition of microsomal PG responded more quickly to temperature stress than that of chloroplasts (Lynch and Thompson, 1984a.b). If niicrosomal phospholipids are retailored initially in response to temperature stress. then there should be appropriate enzymes present to remove and re-esterify the different acyl groups (Lynch and Thompson, 1984~).The first enzyme needed would be a phospholipase A and, indeed, such an enzyme has been reported in D..su/inu (Norman and Thompson, 1986). Microsomes, but not chloroplasts. contained a fatty acyl hydrolase with high activity towards endogenous or exogenous PG and PE. The enzyme had little activity towards other phospholipids or MGDG. Because no monoacyl products could be detected, it was not possible to analyse independently the activities of any specific enzymes, such as phospholipase A , or A,, or lysophospholipase which might be present. Lipolysis was most active in the presence of 10 mM C a 2 + , and was enhanced by calmodulin and inhibited by calmodulin antagonists, such as W-7 or 48/80. Most interestingly, the acyl hydrolase activity of 30 C-grown cells was low when measured in vitro at 12 C. However, when cells were chilled to 12'C, activity as measured at 12 C in vitro rapidly increased, thereby providing the mechanism for retailoring phospholipids during low-temperature acclimation. The low acyl hydrolase activity in chloroplasts from similarly treated cells emphasized the key role of micro-

27

LIPID METABOLISM IN ALGAE

18:1/16:0 MGDG

18:2/16:0 DGDG 18 1/16 1 MGDG

18 1/16 1 DGDG

18 3/16 0 DGDG

D' s

18 3/16 4 MGDG

>18

3/16 4DGDG

l i g . 9. Pathways for galactosylglyccridc synthesis in Diititrlidltr plasts. Redrawn from Cho and Thompson (1987) with permission.

.srr/inti

chloro-

soma1 metabolism in temperature adaptation (Norman and Thompson, 1986). Although the labelling of galactosylglycerides in D.siilinu has not been studied in as much detail as that of the phospholipids. a recent report describes labelling of molecular species from I4C-labelled fatty acids (Cho and Thompson, 1987), and a fatty acyl hydrolase preferentially attacking MGDG has been reported (Cho and Thompson, 1986). The results of the labelling studies are summarized in Fig. 9. They showed that, as expected (Harwood, 1988), the initial molecular species of MGDG labelled by &novo synthesis was the 18 : 1/16 : 0. This molecular species could then be further desaturated at both positions to eventually produce the highly unsaturated 18: 3/16:4 species. However, after the initial desaturation to 1 8 : 1/16: I , this species (like others) of MGDG was a substrate for galactosylation. The DGDG so produced was itself a substrate for continued desaturation. The 18 : 1/16 : 0 species of MGDG could be galactosylated but the DGDG so produced could only be desaturated at the sn-l position to yield a-linolenate. No further metabolism of palmitate at the sn-2 position took place (Cho and Thompson, 1987). These observations are particularly interesting because not only do they provide further evidence for the involvement of complex (galactosylglycerides) lipids as substrates for desaturations, but they also confirm that ( I ) lipid-linked acyl chains can be subject to a whole series of desaturations and ( 2 ) that several lipid types (in this case DGDG as well as MGDG) may serve as substrates for an individual desaturation. These topics are reviewed more fully in Harwood ( 1 988).

28

JOHN L. HARWOOD A N D A. LESLEY JONES

VII.

METABOLISM I N MARINE ALGAE A.

LABELLING CHARACTERISTICS

There have been relatively few studies on the lipid metabolism of marine macroalgae. There is now, however, a considerable body of work on their lipid and fatty acid compositions. Earlier work in this area has been summarized by Pohl and Zurheide (1979a). Most of the lipids which are found in marine algae occur in higher plants, although there are exceptions, and marked contrasts are seen in the lipid patterns of different algal divisions (Table IX). Marine algae have a characteristic pattern of polyunsaturated fatty acids which is quite distinct from that of higher plants (see Section Ill), and again reflects differences among the algal divisions (Pohl and Zurheide, 1979a). These observed differences in marine algal lipids and fatty acid content are presumably a reflection of differing metabolism, but there is very little detailed information available. The marine algae typically contain high proportions of polyunsaturated fatty acids (e.g. Jamieson and Reid, 1972; Pohl and Zurheide, 1979a). The brown and red algae contain arachidonic (20 : 4. w-6,9,12,15) and eicosapentaenoic (20 : 5 , w-3,6,9,12,15) acids as major fatty acids, with the brown algae tending to have more of the former and the red algae more of the latter. The green algae have only small amounts of C,, fatty acids, but do contain C,, and C , , fatty acids, which are more unsaturated than those of higher plants. Entrromorphu intrstinalis, a marine green macroalga, has among its major fatty acids a-linolenic acid ( 18 : 3, w-6,9,12), which is typical of higher plant photosynthetic tissue, and also octadecatetraenoic (18 : 4, w-3,6,9,12) and hexadecatetraenoic ( 1 6 : 4, w-3,6,9,12) acids (Jones and Harwood, 1987). Octadecatetraenoate is found in some higher plants, e.g. borage (Stymne rt ul., 1987). In this species, octadecatetraenoate is formed from cz-linolenate while esterified to MGDG (Griffiths et al., 1988). Labelling studies on the fatty acids of algae using [I4C]acetate show that the major fatty acids labelled are generally palmitate and oleate. Incorporation of radioactivity into palmitoleate, stearate and the more polyunsaturated C ,, fatty acids with long-chain C,,, C,, and occasionally C,, saturated fatty acids (Table X), is usually seen also. This indicates that the initial pathway of fatty acid synthesis is similar to that of higher plants, but that additional desaturase and elongase enzymes must be present for the production of the complete marine algal fatty acid pattern. The long-chain polyunsaturated fatty acids are themselves synthesized slowly, as indicated by time-course studies for up to 24 h with [I4C]acetate, when n o radiolabel accumulates in arachidonate or eicosapentaenoate (Jones, A. L. and Harwood, J. L., unpublished). A preliminary report for Porphyra yezoensis suggests a route for chain elongation and desaturation in this alga, but further studies are needed to confirm this (Kayama et al., 1986).

TABLE IX The lipid composition of marine algae representing different algal divisions Lipid

Phaeophyta

Rhodophyta

Chlorophyta

F. serratus

F. vesiculosus

Ascophyllum nodosum

Chondrus crispus

Polysiphonia lanosa

E. intestinalis

MGDG DGDG SQDG X

18.1 23.1 32.9 7.5

15.0 11.3 22.0 24.1

19.7 16.6 19.4 17.2

17.6 12.8 14.7 n.d.

17.6 24.6 11.9 n.d.

45.9 14.8 14.8 n.d.

PC PE PG PI DPG DGTS

4.3 5.7 2.5 2.1 4.2

4.2 6.2 2.2 2.9 5.4

3. I 9.8 1.5 2.5 3.1

31.6" 1.8 8.2

18.3" 1.5 5.0

-

-

-

4.9

5.0

7.6

15.0

1.8

2.1

1.8

2.7

NL

Rest

1.6

Data as means n = 3-7; X, unidentified glycolipid; n.d., none detected. Results expressed as YOtotal lipid "PC+ PSC

-

1.5 -

2.6

1.5

-

13.7

3.3

30

J O H N L. H A R W O O D A N D A. LESLEY J O N E S

TABLE X Rudioluhelling

(?f:firttj'acids f r o m

[ ' 4C]uce1ate in various marine algae

Fatty acid (YOtotal fatty acids) 1 4 : 0 16:0 16.1 18:O 1 8 : l 1 8 : 2 2 0 : 0 22:O Others Phaeophyta F. si~rrutiis 5 F. i~e.cicu1osu.c 3.4 A.vc~op/ivlluninorlosion 2.6

42.0 16.0 19.9

Rhodophyta C'honclrus c ~ i ~ p t i . s Polj~siphoniuItrrro.srr

I .5 6.5

5.7 40.9

Chlorophyta E. intc.stinu1i.s

1.7

9.8

13 I 17 1.8 12.1 41.1 tr 11.6 43.3

2 3.8 4.8

6 5.3 4.0

12.0 10.9

3.8 62.6 7.2 21.5

4.3

3.5 4.8

2.8

2.2 42.1

9.2

~

2.9

10 8.9 9.2

4 7.7 4.1

4.6

2.8

~

~

8.7

16.5"

" ~ 1 83: + IX.4: tr

= 160 km h- l ) failed to strip deciduous trees of their leaves. As a consequence, many mature trees were uprooted or suffered breakage of the trunk or major branches. Had the leaves been more easily shed, trauma would have been less severe because of the reduced wind resistance offered by naked branches (cf. volcanic eruption effects). The day after the storm I observed the River Medway nearing bank-full

112

ROBERT A. SPICER

discharge transporting numerous leaf-bearing branches. Isolated floating leaves were not as numerous as one might have expected. Fallen trees (e.g. Fugus, Quercus, Populus, Tiliu) retained their leaves for several weeks, and leaves remaining on upright deciduous trees were blackened and desiccated, and in some cases tattered, but again remained on the trees for several weeks. From these observations one might postulate that sedimentary deposits resulting from this storm would have a limited flora, but had the storm occurred a few weeks later, when more leaves would have been shed or more easily stripped from the trees, leaf accumulation would have been considerably greater. It follows from this that storm damage to predominantly evergreen vegetation is likely to be routinely marked by a high proportion of broken branches and trunks and forest damage. The quality of leaf, fruit and seed assemblages formed under these conditions is difficult to predict, and more work is clearly needed on this aspect of plant taphonomy. In temperate regimes with mostly deciduous vegetation, storm damage effects will be strongly dependent on the timing of the storm in relation to foliar condition. Several fossil assemblages have been specifically ascribed to storm (wind) effects (e.g. Potonie, 1910; Wnuk and Pfefferkorn 1987). The usual criterion for recognizing such deposits is directional tree blow-down in the absence of fluvial or volcanic sediments that could provide alternative explanations for log orientation.

IV. LITTER DEGRADATION ON THE FOREST FLOOR In an earlier publication (Spicer, 1981) I implied that mechanical degradation of dry leaves in subaerial environments was likely to be minimal. Although in general this remains true, Ferguson (1985) reported the results of experiments which show that this need not be the case. Ferguson tumbled a selection of dry leaflets of Aesculus hippocustanum for a period of 2 weeks in a 20-cm diameter drum at 100 rev min-*. The result of this somewhat harsh treatment was the attrition of intervascular tissue until mostly only the primary and secondary veins remained. Dry leaves tend to be rigid and brittle and thus predisposed to collision breakage. They also tend to be curled, which enhances their transportability by wind. In most circumstances litter will be moist at the time of abscission or become wet soon after landing on the forest floor. High moisture content tends to render leaves flexible and as a result they tend to lie flat on the substrate and suffer less lateral wind transport. If the surfaces of the leaves are wet they will tend to stick to each other and to the substrate. Moisture also predisposes the leaves to bacterial and fungal degradation, particularly if precipitation leaches out water-soluble polyphenols that tend to inhibit decay. According to Ferguson (1989, the composition of the saprotrophic community, and therefore decay rate, is determined by climate, the nature of the

FORMATION A N D INTERPRETATION OF PLANT FOSSIL ASSEMBLAGES

1 13

Fig. 6. Diagrammatic section through a gallery forest bordering a river showing principal sources of litter (stippled) sampled by the river. The forest on the left is shown supporting a dense growth of climbers that dilute the litter contribution from forest trees. (Modified from Ferguson. 1985.)

substrate, and the composition of the litter. To this one must add the geological time period because evolutionary development of the community is also likely to play a significant role. Decay on the forest floor is highly selective. Experiments with mixed species of leaves in nylon mesh bags (Ferguson, 1985) showed that while some species (e.g. Fagus sylvatica, Platanus x hispanica) suffered little decay after I5 months, other taxa (e.g. Acer pseudoplatanus, Alnus gfutinosa) were skeletonized. Ferguson suggests that the overall composition of the litter will affect which elements are selectively lost in that litter that is primarily composed of resistant species, moderately resistant taxa will be preferentially destroyed. On the other hand, in a situation where easily degraded taxa predominate, the moderately susceptible species preferentially survive. Similarly, the degradation sequence will be determined to a large extent by litter composition. In some circumstances these differences in decay rates may be linked to specific vegetational components. For example, in Puerto Rican montane rainforest, litter decay is faster in principal successional taxa forming the uppercanopy than in secondary taxa (La Caro and Rudd, 1985). Once a plant organ is incorporated into forest-floor litter, its capacity for entry into an aquatic sedimentary environment is reduced greatly. Some material is blown laterally into stream systems and lakes (Fisher and Likens, 1973), but as discussed above, this contribution is small if the vegetation is closed, although it may be more significant in more open environments (Ferguson, 1985). Vegetation bordering open water, where the forest canopy is broken, tends to be rather dense (Richards, 1966), presumably due in large part to increased light levels. This creates a wall of riparian vegetation often specialized with a high proportion of climbers, which not only filters out litter produced by (and more representative of) the forest as a whole, but also contributes large quantities of debris of its own (Fig. 6). Undercutting of river banks by channel migration or bank-full discharge

114

ROBERT A. SPICER

leads to direct input of forest-floor litter, much of which is likely to be partly degraded and partly water saturated. In many instances live herbaceous ground cover is also introduced into river systems (Figs 7 and 8). The introduction of such material to sedimentary environments enriches greatly the potential fossil assemblage, not only in terms of the quantity of organic debris but also in terms of organ and species richness (Spicer, 1980; Spicer and Wolfe, 1987). Indeed, many organs that do not normally enter allochthonous assemblages (e.g. roots and heavy seeds/fruits or branches and that have a limited capacity for lateral dispersal) may be represented. However, the mixing of litter from one location with that from another, the selective degradation processes that operate on the forest floor, and the mixing of forest-floor litter with relatively fresh material, are all likely to generate an assemblage that can only be regarded as a bulk sample of vegetation within the drainage basin as a whole (Spicer and Wolfe, 1987). Bank erosion is also responsible for the frequent introduction into river systems of whole living trees (Fig. 8a). When this occurs, leaves and most branches are stripped from the trunks, which may sink to the river bed and be deposited as part of a basal lag or stranded on banks or bars. Typically the flared root systems survive abrasion enough to encounter the river substrate. The still floating log then swings around in the flow so that the upper part of the trunk points downstream (Fig. 8b). The absorptive capacity of root systems persists after death, so that logs with roots attached tend to sink root end first (Greer, unpublished data). This not only contributes to “root stranding” but can give rise to apparent “in situ” forests with transported trees in life position provided that water depth is great enough and flow is virtually non-existent. This phenomenon has been noted in lakes surrounding Mount Saint Helens, where many trees were snapped by volcanic blast several feet above ground level before being blown or washed into the lakes (Coffin, 1983). In contrast, bank collapse seldom results in snapping or preferential rotting of the trunk a short distance above the root system. Instead, long lengths of trunk survive. The ratio of trunk length to root base diameter of these logs dictate that their most stable configuration is horizontal. The discovery of upright tree bases in non-volcaniclastic sediments suggests strongly that the trees have been preserved at their site of growth by inundation of the forest by sediment. In volcanic terrains the situation is very different and will be discussed in detail later.

V. AQUATIC PROCESSING OF PLANT DEBRIS The entry into an aquatic environment brings about profound changes in material derived from terrestrial sources. The following discussion will be based on the assumption that the material under consideration has been dir-

FORMATION A N D INTERPRETATION O F PLANT FOSSIL ASSEMBLAGES

1 15

Fig. 7. (a) Aerial view of floodplain depositional complexes showing both active and abandoned channels (Yukon River floodplain, central Alaska); (b) bank collapse introducing trees from mature floodplain communities; (c) community heterogeneity on successive floodplain accretionary surfaces.

ectly transported to the water surface by wind. Similar processes operate on detritus that has been in the forest-floor environment before entering the aquatic realm, but partial saturation, leaching, and decay processes will have already taken place to a greater or lesser extent. A.

INITIAL PROCESSES-FLOATING

Immediately upon landing on the surface of a body of water, plant material,

116

ROBERT A. SPICER

Fig. 8. (a) Detail of active bank erosion exposing interfiuve vegetation in vertical cross section from which litter derived from all forest strata can enter the river (Yukon River, central Alaska); (b) bar-stranded whole trees alligned parallel to flow with root balls facing upstream, flow is from right to left (Yukon River, Alaska).

e.g. a leaf, begins to absorb water and soluble substances begin to be leached out. Initially a dry leaf will float and may remain buoyed up by surface tension for considerable periods of time (more than several weeks), provided only that the bottom surface of the leaf is wetted and the water surface is calm (Spicer, 1981). Conceivably, plant material could be transported long distances this way, but such conditions are only likely to pertain in slowflowing rivers protected from wind (i.e. subcanopy streams). These are situ-

FORMATION AND INTERPRETATION OF PLANT FOSSIL ASSEMBLAGES

117

EXPLANATION No agitation of surface water

h

Frequent agitation of surface water

40

80

120

i0

TIME, I N HOURS

Fig. 9. Fugus sylvuricu leaf floating times (from Spicer, 1981).

ations in which long-distance transport is unlikely to occur because of small stream size. The uptake of water by leaf tissues is governed by cuticle and epicuticular wax thickness, abundance of stomata and/or hydathodes, damage to the lamina or petiole and water temperature and chemistry (in particular oxygenation (Spicer, 1981; Ferguson and De Bock, 1983; Ferguson, 1985)). Leaf anatomy may also be important (Ferguson, 1985; Greer, unpublished data). In view of these variables, and incomplete preservation in fossils that only rarely allows quantification, several workers have set out to establish ranges of floating times in order to evaluate the likely role of differential floating in assemblage formation. Typically, experiments have been conducted in aquaria with moderate frequent agitation to simulate wave action. Spicer (1981), Ferguson and De Bock (1983) and Ferguson (1985) have all noted that floating times range from several hours to several weeks, with thin chartaceous (papery) leaves tending to sink first, and thick coriaceous (leathery) leaves floating the longest (Figs 9, 10 and 11). Because individual leaves within a population exhibit a range of floating times that follows an “S”-shaped curve, the most useful statistic for comparing floating times is the “half-life” (Ferguson, 1985). Present results suggest that lamina damage (holes) and petiole loss both decrease floating times. According to Ferguson (1985), the leaf stalk of compound leaves acts in much the same way as petioles on simple leaves in that it takes longer to saturate and buoys up the leaf. Thus intact compound leaves float longer than their individual leaflets. The floating times of dispersed fruits and seeds (diaspores) have also been investigated from the view of both reproductive dispersal (Praeger, 1913; Ridley, 1930) and taphonomy (Collinson, 1983). In general, diaspores exhibit

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a greater range of floating times than do leaves. Floating times do not appear to be related directly to diaspore size because small seeds can remain afloat for several weeks. Floating times seem unrelated to the habit of the parent plant (Collinson, 1983). Wood and, in particular, logs can remain afloat for several years (Spicer, personal observation; Coffin, 1983), and potentially, therefore, the only hindrance to log dispersal throughout a drainage system downstream from the growing point is water (channel) depth and instream obstacles. In particular, where ancient channel deposits suggest water depth was adequate for log transport, and yet no large logs are found in spite of an abundance of other

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plant remains, there is a real possibility that large trees were absent from the community. The long floating times of logs also raise important questions regarding the use of fossil tree rings for climate interpretation when the trees in question are preserved in marine sediments. Today the western end of the Alaskan Peninsula is treeless and yet the beaches are littered with thousands of drifted logs. These trees are derived in large part from the area of Japan and therefore carry an allochthonous climate signal. Although floating transport of plant debris is obviously an important factor in mixing material derived from different source communities, all the while a plant organ is protruding from the surface of the water or lies in the surface waters it is also subject to the effects of wind. In this way material can be moved across a lake (often several times) before sinking, and rivertransported material may be blown to the sides of the channel where it may become stranded. B. TRANSPORT IN THE WATER COLUMN

Once the specific gravity of any object in fresh water exceeds unity, that object will sink. In most plant material this condition is achieved by progressive water absorption. Progressive saturation follows an “S”-shaped curve and does not cease until long after the object has sunk (Greer, unpublished data). Progressive post-sinking water absorption continues to affect the submerged density of the object (and therefore its behaviour during transport in the water column) until the condition of full saturation is reached. When and where the object eventually settles is determined to a large degree by submerged density and shape: two factors that are important in determining settling velocity and entrainment behaviour. When submerged, an object may be moved while being suspended by turbulence in the water column or by rolling and bouncing (saltation), or by gliding along the stream bed. The length of time a plant organ is transported in these modes depends largely on its settling velocity and the rates of water flow. Settling velocity also determines to a large extent the depth distribution of suspended solid materials in the water column. In general this distribution is logarithmic, but the complex interaction of the planar shapes of many plant parts with the turbulent eddies present in most natural flow regimes prevents the detailed modelling of this distribution for organic debris. Nevertheless, a knowledge of the relative magnitudes of plant organ settling velocities is necessary to assess relative sorting potential. 1 . Settling (Fall) Velocity in Water Settling velocity of fully saturated plant organs has been investigated experimentally (Spicer and Greer, 1986; Greer, unpublished thesis) using a 2 x 2 x

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2 m settling tank. In spite of their irregular two-dimensional shapes, angiosperm leaves exhibit a surprising degree of within-taxon uniformity of settling velocities, as do more prismatic shapes of conifer needles (Fig. 12). Even very irregularly shaped material, such as isolated fern pinnules and moss leafy shoots, have fall velocities that fall within narrow, moderately welldefined limits (Fig. 12). Statistically, no significant difference exists between the fall velocities of different broad-leaved taxa (including Ginkgo and fern pinnules), but significant differences do exist between conifer needles and broad-leaved taxa, and among individual conifer taxa (Greer, unpublished thesis). On the basis of these results one might expect no substantial hydraulic sorting to occur among angiosperm taxa, where sorting would be related strongly to settling velocity (e.g. in a flow velocity gradient over a fluvio-lacustrine delta slope). On the other hand, leaves of conifers are likely to be separately deposited from angiosperm leaves derived from the same community: a phenomenon that has been observed in the field (Spicer and Wolfe, 1987). In general, conifer needles have higher settling velocities (e.g. 3.03 cm s-' for Piceapungens at full saturation) than angiosperm leaves (e.g. 1.5 cm s - ' for Fagus sylvatica at full saturation), although individual leaves of other broad-lamina taxa such as Ginkgo biloba sometimes exhibit fall velocities as high as 6.7 cm s when petiole and lamina configuration produce a hydrodynamically efficient shape that results in a stable gliding fall. The extension of these studies to diaspores and fragmented leaf material would prove most valuable. 2. Entrainment and Burial For any given flow rate, particles concentrated near the stream bed will be

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mostly those with the greatest settling velocities. The heaviest particles will be transported as bedload and be in suspension only for brief periods of time. As current flow wanes, the lighter fractions will progressively settle out. Conversely, increases in current flow progressively entrain material. Flow rate in natural streams and rivers is rarely constant and plant debris is likely to undergo several cycles of deposition and entrainment before permanent burial takes place. Deposition and entrainment of plant particles is a complex and as yet poorly understood process. For less variable, flakey inorganic particles such as mica, experimental results have been ambiguous (Schoklitsch, 1914; Shields, 1936; Pang, 1939; Mantz, 1973, 1977; Berthois, 1962), even though plane sedimentary beds (defined as plane to within one solid particle diameter) were used. Leaf orientation and aspect in relation to fluid flow will clearly determine the flow velocity at which entrainment will take place. Curved leaves or planar particles that are inclined with their raised edge facing into the flow will be picked up at lower flow rates than those that are flat on the stream bed or inclined with their raised edge pointing downstream. Indeed, inclination at this latter orientation will result in higher stream velocities merely pressing the object more firmly onto the stream bed until turbulent eddies disrupt the particle, or scour around the particle allows flow to occur beneath it. Bed roughness clearly plays a major role in particle entrainment. By means of flume experiments, Greer (Greer, unpublished thesis; Spicer and Greer, 1986) has been able to show that not only bed particles but also bedforms play an important part in entrainment sorting. If the bedforms (e.g. ripples) were large enough for the particles to settle in the troughs, they were protected from entrainment and often buried rapidly by bedform migration. Larger particles were cleanly swept through the system. Thus, for example, if ripples are noted in a fossil deposit, and only conifer needles are preserved, it cannot be assumed that angiosperms were not present, even in large numbers, within the source vegetation. They may have been deposited elsewhere because they were too large to be trapped between the ripples. By means of flume experiments, Rex (1985) investigated the burial of selected plant debris in simulated stream flow. Migration of bedforms was the main mechanism of stem burial but this played only a partial role in hollow stem infilling. Rex found that sediment in suspension entered prostrate hollow stems as steep-fronted wedges infilling from both open ends even when the stem was aligned parallel to flow. The degree of infilling was dependent on the dimensions of the hollow void, and in particular the diameter of the void in relation to its length. Rarely did long, narrow stems fill completely, because closure of the open ends by sediment prevented sediment penetration to the midsection of the stem length. By means of dye experiments with glass tubes, Rex (1985) showed that the process of infilling was governed by flow separation and vortex generation induced by restriction of flow as the fluid passed over and through the stem tube. Tubes with one end

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closed (caused, for example, by stem nodal diaphragms, crushing, or abutment to bedforms) reduced infilling further, and blocked tubes never completely filled under the conditions operating in the flume. In Rex’s (1985) experiments, sediment transported as bedload filled stems orientated parallel to flow in a somewhat different fashion, in that the infilling sediment wedges had a less steep leading edge, and showed a distinct graded structure favouring the deposition of the coarser sediment fractions. Infilling of stems oriented with their long axis not parallel to flow was similar to that seen with suspended sediment, but the structure and degree of infilling was not as constant and depended on stem orientation and length. Comparisons with fossil stem fills (Rex, 1985) showed that this approach was valid and provides a potential method of determining the sedimentological regime during burial. However, as Rex (1985) points out, the incomplete filling of tubes with a closed end poses real problems in the interpretation of completely infilled fossils such as the stigmarian root systems seen in the Fossil Grove, Victoria Park, Glasgow (cf. MacGregor and Walton, 1948). Gastaldo et al. (1987) observed that flooding of lowlands is not usually accompanied by a leading “wave” of water, but occurs by raising of the water table. The resulting gradual inundation saturates most of the plant litter before flow rates become strong enough to transport the organics. As water flow increases to peak flood stage, transported inorganic sediment is trapped by the still. in situ saturated mat of forest-floor litter. This actually enhances sedimentation rates and thus burial of the plant litter. Similar processes probably takes place on organic-rich channel bottoms and may be responsible for the incorporation of leaf beds into the sedimentary package (Gastaldo et al., 1987).

C. LEAF DEGRADATION

I . Biological Most leaves entering an aquatic environment become decayed or damaged before they are deposited. Immediately upon entering the water, soluble compounds such as sugars, various mobile elements (e.g. potassium) and some polyphenols (decay-limiting compounds) begin to leach out, and within days leaves reach equilibrium with the chemistry of the surrounding water (Nykvist, 1962; Spicer, 1975). If the polyphenols are in the condensed or insoluble form, their antifungal and antibacterial properties can delay microbiological degradation (Bennoit et al., 1968; Williams, 1963). Leaves most susceptible to microbiological decay are those that have low lignin content, no or few condensed polyphenols, and a high sugar content at abscission (e.g. Alnus). Fungi and bacteria typically enter a leaf through stomata, lamina damage, or the petiole, and preferentially attack the internal tissues of the leaf. Fungi appear to be more important in leaf decay (Kaushik and Hynes,

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Fig. 13. (a) Typical patterns of leaf degradation caused by large particle invertebrate feeders; (b) typical patterns of leaf degradation caused by mechanical abrasion; (c) typical patterns of leaf degradation caused by microbial degradation.

1971). Where the cuticle is thick, all that may remain is an intact bag of cuticle (Spicer, 1981). However, the cuticle is not immune to breakdown, and when this occurs attack typically begins with the surface originally in contact with the epidermal walls, and the cutin of the anticlinal walls is the first to be degraded (De Vries et al., 1967). In leaves with thin cuticles, the cuticle tends to pull away in strips, and, because the spongy mesophyll is less resistant to degradation than the palisade tissue, the lower cuticle is often lost first (Ferguson, 1985). Colonization of the leaf tissues by fungi and bacteria also preferentially predisposes the leaf to attack by invertebrates (Kaushik, 1969; Petersen and Cummins, 1974). The type of degradation caused by invertebrates may be classified into that produced by large-particle feeders (rounded holes and arcuate damage to lamina margins) and small-particle feeders (removal of intercostal tissue and leaf skeletonization) (Fig. 13a,c) (Yonge, 1928; Petersen and Cummins, 1974). As with forest-floor degradation, the species mix will determine the extent to which any particular species is attacked, but in an aquatic system food sources other than terrestrially derived litter may be available. The presence of aquatic plants, and macrophytes in particular, greatly affects the benthic fauna by oxygenating the water and providing food and shelter (Rau, 1976; Ferguson, 1985). If alternative food supplies are available, invertebrates may not degrade leaf litter to any great extent (Webster and Waide, 1982; Dane11 and Anderson, 1982). Trophic state was considered by Ferguson ( 1 985) to be an important factor in selective leaf degradation. Ferguson postulated that in oligotrophic lakes, the generally low nutrient status would force micro-organisms to seek out leaf material, which in turn would lead to destruction by invertebrates. Leaf species rich in nutrients would be preferentially degraded. In eutrophic systems, however, the general availability of nutrients would lead to less species-selectivedegradation, although there is some evidence for enhanced leaf degradation in the presence of high nitrogen and phosphate availability

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(Hanlon, 1982; Newbold et al., 1983; Mathews and Kawalczewski, 1969; Kaushik and Hynes, 1971). Ferguson (1 985) also considered briefly the effect of temperature on leaf degradation and underscored the long-held assumption that decay proceeds more rapidly under warm, rather than cool, aerobic conditions. Invertebrate abundance is adversely affected by high sedimentation rates (Webster and Waide, 1982), and in unstable (i.e. rapidly fluctuating) regimes frequent disturbance is likely to keep population levels low. High sedimentation rates also lead to rapid burial of plant debris (and therefore isolation from invertebrate attack) and, particularly if the sediment is fine-grained, the development of anaerobic conditions. Oxygen depletion around the organic material is essential to preservation because this slows and eventually stops the decay processes. 2. Mechanical Degradation Waning water flows will commonly result in intervals of rapid sedimentation. Intuitively one might think that high energy flow regimes would degrade most plant material, but experiments using tumbling barrels (Ferguson, 1971, 1985; Spicer, 1981 ) show that even comparatively delicate plant organs such as leaves are remarkably robust when freshly abscised. However, leaves that have suffered even the slightest amount of microbiological attack are weakened substantially (Spicer, 198 1). The degree of mechanical fragmentation that takes place for any given flow regime and instream obstacle density is a function of the decay state of the leaf and its structure. These two factors are, of course, related and, as we have seen, decay is a function of a variety of environmental factors. The robustness of fresh leaves has been used as one line of evidence for the existence of wholesale deciduousness in Cretaceous near-polar forests. Spicer and Parrish (1986) examined a wide range of sedimentary facies in Late Cretaceous rocks on the North Slope of Alaska. In all sediment types, even fluvial sandstones, none of the leaf material exhibited significant biological or mechanical degradation. This was interpreted to mean that all the plant material was incorporated more or less simultaneously while fresh, and therefore as evidence of synchronous leaf fall (Spicer, 1987). Mechanical fragmentation is characterized by angular breaks and tears in the lamina and is quite distinct from damage brought about by biological agents alone (Fig. 13b). The presence of such damage in fossil leaves is strong evidence that they have undergone stream transport, and in favourable circumstances degradation studies may be used to differentiate growth sites. Such a situation might be the deposition of mechanically degraded, streamtransported leaves in a lacustrine setting where local taxa have suffered only biologically induced damage. Mechanical degradation of diaspores with hard protective coats is usually slow to occur (Collinson, 1978) and diaspores are, in general, more robust

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than leaves. Here again biological degradation is critically important and may well be the main agency for diaspore destruction (Collinson, 1983).

VI. FLUVIAL TRANSPORT River systems provide the route by which most larger plant organs may travel the greatest distance from the growth site. The size of the drainage basin and the volume and speed of water moving through the system will determine the maximum distance that any given plant particle may travel, but in reality this potential is seldom realized. The headwaters of a river are usually in areas of moderate to extreme topographic relief. This topography provides a wealth of edaphic and climatic environments in which vegetation of considerable heterogeneity can exist. Communities specific to certain altitudes or aspects can coexist within short distances of one another, and contribute litter to streams flowing past them (e.g. Spicer and Wolfe, 1987). The detritus from these distinct sources is mixed during fluvial transport over relatively short distances, and any resulting deposit provides a summary sample of the communities growing within the drainage basin (Spicer and Wolfe, 1987). Not all the communities are equally represented, however. Intermittent stream flow at the periphery of drainage basins exposes plant debris to wetting and drying cycles, stranding and entrapment on rough stream beds that quickly degrade even the most robust of plant material. Even where streams are permanent, high-velocity flow over rough substrates can impede transport. Greer, in Spicer and Greer (1986), reported the results of leaf transport experiments carried out in the devastated posteruption blast area of Mount Saint Helens (Washington, USA). In these experiments 1000 fully saturated and 1000 air-dried leaves of Fugus sylvuticu were released into a small stream system 1.2 km from its termination in a fluvio-lacustrine delta. The maximum flow velocity of the stream was 1.1 m s - l (corresponding to the narrowest-2.8 m wide-part of the channel), and the minimum velocity was 0.52 m s C 1 (channel width 15.5 m). The deepest part of the channel was 0.35 m at its narrowest point. Even under these ideal conditions, with no riparian or aquatic vegetation, only 0.2% of the unsaturated leaves, and none of the saturated leaves, reached the delta within 48 h after release. Entrapment occurred by stranding on the stream margins (mostly unsaturated leaves) or by imbrication against stream-bed obstacles (mostly saturated levels). In this instance, stream-bed obstacles consisted entirely of cobbles or gravel. In a normal vegetated environment, stems and branches would pose additional obstacles. Over time, the median point of each population moved downstream, indicating that many leaves were trapped in a metastable configuration, and could have been flushed further along the stream with increases in flow rate, but the time taken for any appreciable

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transport to occur exceeded that at which biodegradation substantially weakened the tissues and rendered them susceptible to mechanical break-up. The main factor in limiting downstream transport appears to be water depth and stream-bottom roughness in relation to the size of the plant particle. Small, high-energy streams occur in areas of greatest relief where depositional environments are generally considered rare. Tributary systems are erosive and a long way from depositional environments. The exceptions are intermontane basins in which plant remains are preserved in lacustrine sediments. Typically a valley may become dammed by a landslide or volcanic activity (lava or debris flow), resulting in the formation of a lake. Stream flow contributes inorganic sediment, and plant material and delta complexes result that reflect strongly the slope communities. The nature and value of these deposits will be discussed later. Although the potential for long-distance transport of meaningful samples of hinterland vegetation is severely limited in small, high-energy tributary systems, the situation is somewhat different in larger fluvial regimes (Ozaki, 1969). Several types of river have been recognized based on their generalized geometry (Allen, 1965, 1978; Bridge, 1984; Miall, 1982; Smith, 1983; Schumm, 1981). Braided rivers tend to form where discharge is highly variable and sediment load is often high (e.g. in glacial and seasonally arid environments), whereas highly sinuous (meandering) rivers are seen in lowenergy situations where flow and sediment load fluctuate little (floodplains with little seasonal variation in water supply). Topographic gradient, sediment supply, bedrock characteristics (in erosive settings) and climate are key elements in determining river channel course. These factors, and river geometry, determine the types of depositional subenvironments (channels, etc.) associated with the fluvial regime, and hence the quality of the plant fossil record in relation to the source vegetation. A. CHANNEL DEPOSITS

Water flowing along a natural channel does not move at a uniform rate. Frictional forces along the channel bed cause the water in contact with the channel boundaries to flow more slowly, and a vertical section through a channel, parallel to the axis of Bow, normally reveals a logarithmic distribution of flow velocities. Instability in the flow regime and natural obstacles cause river channels to become sinuous or to anastomose. Furthermore, whenever water flows around a curve, water on the inside of the bend flows more slowly than that on the outside of the curve. These differences in flow velocity lead to deposition and winnowing of sediments in different parts of the channel. Lag deposits form on the channel bottom (Figs 1 , 2 and 14) and are mostly composed of coarser material with the highest settling velocities. This material comprises the largest clasts that were being transported as part of the bed-

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Fig. 14. Hypothetical vertical section through an infilled abandoned channel. a, basal channel lag deposit containing logs from channel margins especially where channel sinuosity has resulted in bank erosion; b, early phase of infill during waning current-litter derived from riparian sources; c-e, successive infilling at repeated flood stages-litter derived from riparian, levee, overbank, and local “ox-bow” margin communities; f, final phase of infill as mire community develops organic-rich clay3 and peat to cap deposit-lateral and vertical changes in peat composition record the development of the mire community.

load, and lies on an erosional surface cutting into the underlying sediments. In a typical river channel with a broad-spectrum sediment supply, a lag deposit would consist of gravels or pebbles in perhaps a coarse sand matrix. Organic sediment would be made up of logs and larger, more robust, fruits and seeds. Occasionally, reworked clay balls containing more delicate plant parts may form part of a channel lag, but in such a case the material in the clay matrix may not have been contemporaneous with that in the rest of the channel sediments. Lag deposits are normally reworked as flow in the channel fluctuates, but they become preserved when the channel migrates laterally or is abandoned. Point-bars are typically (though not exclusively) formed in meandering rivers and are composed of sediments deposited by the slow-flowing water on the inside of channel bends. In many instances they bury and preserve the channel lag. Characteristically, point-bar sediments become finer grained upwards, have lateral accretion surfaces dipping down to the base of the channel, and possess a variety of bedforms, such as ripples, that decrease in scale upwards. The upper portions of point-bars are deposited in water with the least energy and typically contain the most diverse plant remains. Probably the best sample of riparian vegetation is to be found in these deposits, because robust material such as fruits and seeds and coriaceous leaves, as well as delicate elements such as flowers and even seedlings, can be incorporated. As with other depositional environments, the degree to which such material is preserved depends on the activity of the channel (as it affects subsequent erosion and deposition), and the colonization of the point-bar by later riparian vegetation. There can be little doubt that lag and point-bar deposits primarily sample riparian vegetation. However, the degree to which plant remains have undergone long-distance down-river transport before burial is more problematic.

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ROBERT A SPICER

Wide. often deep, channels provide ;I large water surface area and volume for the plant material to move in without becoming trapped by ohst* ‘ i-1~ e so r abraded and fragmented. I n quiet, slow-moving rivers. leaves may be buoyed up almost indefinitely by surface tension (Spicer, 1981 ), whereas whole rafts of plant debris can be carried along, the woodier elements supporting the more fragile and more easily saturated components, even under flood conditions (Berry. 1906). I t is reasonable to assume, therefore, that channel deposits will contain a mixture of plant detritus derived from varying distances upstream. At any given site, however, unless there is evidence for the stranding of a “raft” of vegetation, allochthonous elements will be greatly diluted by material derived from locally growing sources. Levee deposits form naturally when floodwaters. carrying sediment, overtop the rivcr banks and spill out across the floodplain. Release from the confines o f the channel immediately reduces the flow rate, and sediment is depasited lateral to the channel. Successive floods build up a levee that is highcst near thc channel and thins towards the floodplain. This is because the coarsest. bulkiest sediment falls out of suspension first, followed by successively tiner materials as the water flows away from the channel. Levees are composed of laminated sands and silts marked with ripples, climbing ripples and small scours. In vertical section perpendicular to the channel axis they are characteristically wedge-shaped. Because levees are mostly subaerially exposed and relatively well drained between floods, they support different plant communities than the surrounding alluvial swamps (Gastaldo, 1985a,b,c). Oxidation and root penetration tend to destroy most deposited debris, and. in general. levees are poor sites of preservation except, perhaps. for large logs (Gastaldo. 1989; Gastaldo o t LII.1989). In her comprehensive and significant study of fluvial margin litter in paratropical forest environments of southern Mexico, Burnham ( 1 989) reported that low lying areas close to channel margins, the point-bar and levee forebanks. exhibit low species richness and tend to be homogenous. This homogeneity throughout Burnham’s study area must in part be due to fluvial transport mixing of community diversity along the river course. Litter samples reflected well the immediate vegetation in all the subenvironments studied (channel, forebank. levee, back levee), but only slightly less well represented was the local vegetation. As might be expected, the regional flora was the least well represented in all sites because of local dilution effccts. Levee samples represented strongly their own immediate and local f o r a s and back levee sites were more similar to other back levee sites than to other subenvironments. Among Hurnham’s conclusions she pointed out that although within-subenvironment collections were biased, overall and taken together the subenvironments studied yielded a physiognomic signal that reflected well the climate under which the vegetation was growing. Provided that litter collections become incorporated into the fossil record with minimal species (and

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organ) dependent losses, and assemblages from a range of subenvironments are studied, the fossil record is capable of yielding reliable palaeoclimatic signals. This conclusion supports the approach adopted by Spicer and Parrish (1986) and Parrish and Spicer (1988) of multiple facies sampling so as to minimize errors in palaeoclimate reconstruction when strong facies/assemblage association occurs. Crevasse splay deposits are formed when the natural levees are breached in time of flood. The lateral channel that results transports sediment through the gap in the levee and out onto the floodplain. Viewed from above, crevasse splay deposits are commonly fan-shaped with the narrowest portion at the levee breach. The sediments themselves are usually muds, silts and fine sands-the finer fraction of suspended load highest in the river water column. The sediments also tend to become finer away from the point of levee breach. Typically, standing vegetation of the back levee, lateral swamps and floodplain is inundated by the splay deposits. Tree bases may be preserved in situ (Allen, 1970; Gestaldo, 1986a, 1987a), and forest litter may be buried or incorporated into the sediments (leaves are often “rolled” within the sediment matrix), and mixed with river-transported riparian debris and detritus from the levee community. At the sediment-water interface of a crevasse splay in the modern Mobile Delta, Gastaldo et al. (1985) observed that of the 37 taxa identified to species, 34 were not community members of the local vegetation. Rather they were members of either the levee-alluvial swamp or “Pine savanna-bay forest-upland” communities. Only 16% of the recovered macroflora represented local vegetation (Gastaldo, 1985). The speed of burial, the relative fineness of the sediments, and the potential mixture of communities represented, make crevasse splay deposits extremely valuable for obtaining an overall picture of regional floodplain vegetation. This “bulk sample” is particularly useful for palaeoclimatic interpretations, provided the various source communities represented can be resolved by comparison with other more specific, but more local, community samples in other sedimentary facies. The complexity of crevasse splay assemblages is, as yet, poorly understood and more work is likely to yield significant benefits. Floodplain deposits are formed by several processes depending on the nature of the fluvial regime. Low on the floodplain, frequent “levee topping” spills out fine-grained sediments, typically clays and silts, in wide sheets. Here levee, crevasse splay and floodplain deposits may be difficult to differentiate because they are all aspects of the same depositional process. Plant assemblages are similarly complex, but, in general, samples of the interfluve predominate over large areas. Unfortunately such deposits tend to be thin, and subsequent rooting activity and oxidation often destroy any potential plant fossils. Occasionally though, highly siliceous or calcareous seeds may survive (Wing, 1984). However, in floodplains that are waterlogged for most of the time, organic shales or muds typical of marsh environments develop, and delicate, mostly autochthonous, plant parts may be preserved (Wing, 1984).

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Channel migration and relocation (avulsion) over time rework most of the floodplain sediments. This tends to limit the preservation potential of floodplain and interfluve vegetation, and often the only insight into the nature of regional, non-riparian, vegetation may be gained by looking for ubiquitous elements in all the preserved facies. Abandoned channels are a common feature of many fluvial systems. Channel abandonment may occur by meander neck cut-off (so forming “OXbow” type lakes), and by avulsion. Ox-bows can be recognized by their arcuate or crescent shapes, whereas avulsion and chute cut-off produces less curved, more linear deposits. The base of a channel cut-off deposit is usually erosional into the underlying sediments and may contain remnant channel bedload material (Fig. 14). This is often overlain by finer sediment representing the waning flow associated with abandonment. Single-event abandonment is unusual and there may be several periods of reactivation before the channel becomes effectively isolated from the main river. Flood events introduce silts and sands from time to time, and quiet phases between flooding are characterized by fine-grained, laminated sediments typical of lakes. These lacustrine-type sediments may internally fine upwards, but, in general, upward fining is a characteristic of the sedimentary package as a whole. Plant material can be introduced into a channel cut-off, setting throughout the period of infilling. In the basal sediments, riparian debris typical of lag .deposits may be found, passing up into isolated remains of less robust material that was in suspension in the channel at the time of cut-off, or introduced phases of reactivation (Fig. 14). Laminated sediments of quieter periods are likely to contain detritus from communities immediately marginal to the cut-off. In general, low relief and restricted catchment area mean that permanent streams draining into cut-offs are rare, and therefore so too are fluvio-lacustrine deltas. As infilling of the abandoned channel proceeds, water depth diminishes and aquatic communities develop, contributing their own detritus to the potential fossil record. The final phases of infilling are often marked by the development of marsh/swamp communities, and the channel cut-off deposits may be capped with autochthonous organic shales or even coals. Abandoned channel fills including ox-bow lakes, provide a rich source of often exquisitely preserved plant material (Potter, 1976; Crepet and Daghlian, 1981). However, the complexity of the infilling processes demands that detailed sedimentological analysis is required in order to differentiate the contributing communities.

VII.

LACUSTRINE ENVIRONMENTS

Lake basins form in a variety of ways, and the nature of the basin and surrounding topography profoundly affect the nature of the potential fossil

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record they contain. Lakes are so variable that no single suite of sedimentological characteristics is diagnostic of lake deposition. However, several features are more likely to form in lakes than in other environments. Compared to fluvial deposits, lake sediments are laterally more continuous and uniform in thickness. In general they contain fine-grained sediments (though there are many exceptions). They also exhibit extensive areas of fine lamination, and any cross-stratification that exists is of a smaller scale than in fluvial units (Picard and High, 1972; Wing, 1987). However, rapid infilling, particularly of shallow lakes, can produce indistinctly bedded units of relatively coarse sediments that are difficult to identify as lacustrine (Yuretich et al., 1984). The extent to which lake margin (and aquatic) communities are accurately represented in lake deposits depends on basin size and shape, height above the lake surface of the various components of the source community, water chemistry, the amount and distribution of aquatic vegetation, and the characteristics of inflowing streams (if any). If the surface area of a lake is small in relation to the length of its shoreline (e.g. drowned valleys, abandoned channels), the amount of plant debris entering the lake per unit area of lake surface is large, because all parts of the lake are only a short distance from the source vegetation. Furthermore, because the rate of diffusion of oxygen across the air-water interface is a function of the area of the interface (Hutchinson, 1957), the lake tends to become anaerobic with such high organic input per unit surface area, and the preservation potential of the deposited material increases. Source height above the lake surface and distance from the shoreline are critical factors in determining whether or not particular plant parts and taxa are likely to be transported by wind to the lake surface (see Section 1II.B). Spicer (1975, 1981) and Roth and Dilcher (1978) observed selective wind transport to lakes of canopy leaves favouring small, dense “sun” leaves. These leaves are produced at the top of the crown, are exposed to higher wind energies, and are therefore blown further, than “shade” leaves which are produced in the canopy and trunk space. This effect is likely to be most marked where lake width is great in relation to crown height. In such a lake the sediments distal to the shoreline are enriched by sun leaves from canopyforming taxa, and provide a most unreliable sample for community reconstruction and palaeoclimatic interpretations (Spicer, 1981). In such open lake-bottom environments selective biotic degradation of the less robust elements (e.g. shade leaves) is likely to further enhance the bias in favour of “sun” leaves (cf. Heath and Arnold, 1966). Montane lake basins can form as the result of tectonic activity, erosional processes (such as the movement of ice), o r the damning of valleys by slope failure or volcanic activity. The preservation potential of glacial lakes is low because they are generally in an erosional regime, but they frequently survive long enough to be useful for Quarternary studies. The greatest preservation

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potential is found in those lakes resulting from volcanic activity, because the processes that initially dammed the valley can also cap and seal the deposit against subsequent erosion (e.g. Clarkia and Florissant (Smiley and Rember, 1985; MacGinitie, 1953)). Because these lake deposits provide critical insights into not only ancient plant community structure but also vegetation dynamics, they will be treated separately. Isolated lakes ( i t . those with no inflowing or outflowing streams) accumulate plant debris from only two sources: the aquatic vegetation in the lake itself and those communities growing immediately around the lake margins. Low inorganic sedimentation rates are a feature of isolated lakes in that supply is limited to slope wash and surface run-off, aeolian transport. volcanic ash falls, or biogenic sources such as diatom frustules. Although the sediment is usually fine-grained, and therefore ideal for preserving morphological detail, slow influx of sediment inevitably exposes organic material to degradation. Organic deposition accounts for a significant proportion of sediments in isolated lake basins. As infilling proceeds, the ratio of lake perimeter to surface area increases, thus raising the preservation potential of the organics as the system becomes more anaerobic. The eventual fate of any lake is the formation of a swamp, and finally, as more organics accumulate, a forest may develop which is indistinguishable from that which is regionally dominant. Preservation of the debris representing vegetation growing during the final phases of lake infilling is usually poor because of root penetration from subsequent plant communities and oxidation. Aquatic vegetation, although being specialized and of limited palaeoclimatic value, tends to oxygenate the lake water and thereby contribute to the destruction of potential plant fossils. It also traps inwashed (by surface run-off) or inblown plant parts from the lakeside vegetation and prevents forest debris from entering the deeper, and often more anaerobic, parts of the lake. Aquatic macrophytes also increase the abundance and diversity of benthic fauna in the lakes by providing food and shelter (Rau, 1976). The extent of aquatic communities is therefore of particular interest to the taphonomist. Rooted aquatic vegetation tends to flourish (assuming a suitable water chemistry) where water depth is shallow (less than a few metres), water flow is moderate to non-existent, and sedimentation rates are low. Evidence for abundant aquatic vegetation in lacustrine assemblages must imply some considerable bias in the preserved fossil suite because of selective pre-burial degradation, unless other sedimentological evidence indicates that preservation of the assemblage was due to event deposition such as flood or volcanic ash fall. In his review of plant taphonomy in lacustrine sediments Rich ( 1 989) concludes that pollen and spores alone may not give an adequate indication of ancient vegetation and should be supplemented by megafossil data. He also underscores the need to relate sediment type to assemblage composition.

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Ib) m i m g

BOTTOMSET

Fig. 15. Water flow fields over a fluvio-lacustrine delta. See text for details. (Modified from Jopling, 1965a).

Ox-bow lakes have received comparatively little taphonomic attention, but Gastaldo et al. (1989) provide a detailed insight into plant deposition within a Holocene ox-bow lake of the Alabama River. In a transect from backswamp to levee it was clear that the lake sediments themselves preserve leaves as impressions together with organic remains of wood bark, and fructifications. In a separate paper Gastaldo (1989) suggests that in subtropical/ temperate environments such as the Mobile Delta, Alabama, the depositional environment most likely to yield bedded assemblages is in the abandoned channels. A. FLUVIO-LACUSTRINE DELTAS

Perhaps the most valuable lake deposits for the plant palaeoecologist are deltas formed at the mouths of inflowing streams. Not only is the preservation potential of the organic material high because of high sedimentation rates, but also the processes that form fluvio-lacustrine deltas produce plant assemblage patterns that can be used to interpret spatial and temporal aspects of the source vegetation (Spicer, 1981; Spicer and Wolfe, 1987). Upon encountering the relatively static lake waters, the energy of the flowing stream water is dissipated in turbulent flow, the capacity of the stream to transport sediment falls, and deltaic deposits accumulate. Provided that there are no substantial changes in lake level, and the densities of the stream and lake waters are similar, a classic Gilbert-type delta (Gilbert, 1885, 1891) results in which the lake sediments are overlain sequentially by distal deltaic deposits known as bottomsets, followed by toesets, foresets (representing the main part of the delta slope) and finally topsets, which are in effect streambottom sediments. In general the sequence fines upwards and the delta profile is marked in vertical section parallel to the direction of delta advance (progradation) by cross-bed laminations making up the foresets, toesets and bottomsets (Figs 15, 16a). A general model for the formation of this type of delta was proposed by

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Fig. 16. (a) Modern fluvio-lacustrine delta deposits at Trinity Lake, northern California. showing hottomsets. toesets. foresets, and topsets; (h) foreset deposits formed in a lateral lake bordering the Rio Magdelena. Chiapds. Mexic-vertical height of the deposit approximately 3 m.

Jopling (1963, 1965a,b) based on laboratory flume experiments using sand. Jopling envisaged delta deposition by describing the trajectories of individual sedimentary particles as they traversed changing flow velocity fields (Fig. 15). The first field, the “zone of no diffusion”, can be thought of as residual stream flow; following this, particles enter a “zone of mixing” where large scale eddies diffuse the stream energy; and lastly, they enter a zone of reverse circulation where particles are swept back towards the base of the delta slope. A line of zero velocity separates the second and third zones. The point of

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deposition of any given particle (and hence eventually the vertical delta profile) will depend on ( I ) stream depth in relation to lake depth, (2) the settling velocity of the particle, and (3) the velocity of the stream. In particular, the position of the particle in the stream water column as the particle passes over the top of the forest slope and the residence time in the different flow fields are critical factors that determine patterns of deposition.

I . Lowenergy Systems Although originally devised for inorganic particles, Jopling’s model can be used to explain sorting of plant debris in fluvio-lacustrine deltas (Spicer, 1980; Spicer and Wolfe, 1987). Spicer (1981) investigated the accumulation of plant debris in a small, low-energy environment at Silwood Lake, Berkshire, England, and found two distinct leaf beds: one below the delta deposits, representing predominantly lacustrine margin plants, and one at the top of the foresets and in the topsets, representing stream-transported material (Fig. 17). In this system the inorganic sediment fraction was mostly composed of flocculent ferric hydroxide/oxide that had a settling velocity much less than that of the saturated organics. Low stream velocities ( < 1 .O m s - I ) meant that whereas the flocculent inorganics were transported in suspension and as bedload, most of the plant material was moved as bedload only. Consequently the point of greatest organic sedimentation rate was at the top of the foresets, so forming the upper plant bed. The flocs were carried further into the lake basin to build up the delta profile. Progradation of the delta front buried lake-bottom plant accumulations derived primarily from lake-margin communities but also from riparian vegetation upstream, some elements of which were only partly saturated (therefore floating or with a low settling velocity) as they passed over the top of the delta slope. Rapid deposition associated with deltaic sedimentation will bury lakebottom organics and protect some components from the destruction they would otherwise suffer. A similar effect can also be seen in lake sediments normally beyond deltaic influence. In Spicer’s (1981) study, cores revealed that a stream flood event had injected coarse sediment into the lake and produced an upward fining sand-silt-clay horizon that had preferentially preserved taxa normally prone to degradation. Not only did the sand horizon cap lake-bottom accumulations in which partial degradation had already occurred, but also relatively fresh leaves that washed in with the flood sediments became saturated and sank during the time the finer fractions were settling out. These leaves were then buried by the fines before substantial decay could take place (Fig. 18). This example underscores the importance of detailed, high-resolution stratigraphy when interpreting plant assemblages. Plant parts incorporated in an upward-fining cycle that is the result of a single short-term event are likely to be minimally biased by biotic degradation processes. Within the upper plant assemblage, Spicer (1981) was able to map the

136

ROBERT A. SPICER R a n 01 I k a l l y derived leaves

\1

\1

C

- -

*--..---

Vector represenling !he rate 01 sediment depOsilion

Vector representing the late 01 leal deposiliun

Fig. 17. Vector model showing deposition of binary leaf beds in a low-energy Ruvio-lacustrine environment. The lower leaf bed is predominantly derived from sources local to the lake while the upper bed is enriched with stream-transported elements.

lateral distributions of both whole and fragmented leaf taxa, and by using multivariate statistical techniques was able to resolve populations of leaves derived from upstream sources as distinct from more local lake-margin communities. This pattern was most strongly demonstrated in fragmented material (because mechanical fragmentation primarily occurs during stream transport) and led Spicer to propose that analysis of fragmented fossil material was as important in palaeoecological studies as the study of more complete “museum specimens”. So strong was the pattern within the upper leaf bed that in certain instances the position of individual trees relative to the depositional site could be predicted accurately. The two plant beds clearly reflect their separate origins. Plants within the communities local to the lake are represented most strongly in the lower bed, whereas plants in communities at more distant locations are represented in the upper bed. Not only does the species composition differ, but so also does the type and extent of degradation. Leaves in the lower bed will have been primarily transported by wind and subjected to minimal water flow stresses. Consequently the leaves of the lower bed will mostly suffer skeletonization and massive tissue loss produced by biotic degradation. Leaf material in the upper bed, however, will be prodominantly characterized by the angular tears and breaks typical of mechanical degradation. The disparity in species composition between the two beds is not constant. As the delta progrades, its surface will become progressively colonized by various plants as a hydrosere develops. When mature, the delta-top community may well have a composition similar to that surrounding the lake margins (for example, in modern temperate situations Typha, Salix and Alnus are common elements in both environments). Delta vegetation filters

FORMATION A N D INTERPRETATION OF PLANT FOSSIL ASSEMBLAGES DEPTH, IN ORGANIC R E M A I N S METRES

0.0 Leaf B e d 1

0.2

Few leaves dispersed through sediment

0.4

Leaf Bed 2

Well-preserved leaves

INORGANIC SEDIMENT T o p 1.0c m Fe-+hydroxide/ oxide flocs plus some coarse s i l t sized quartz grains Fe++iron-rich sediment as a black semiliquid mud. Clay minerals more o r less absent throughout t h e core

0.6

0.8

Roots in growth posit ion

137

Angular pellets 0.5 c m diameter composed o f same sediments as m u d

1.o

1.2

Black m o r e or less gelatinous m u d Sand layer o f reworked Bagshot sands

Poorly preserved leaves

1.4

Occasional leaf layers

1.6

Fibrous layer remains of aquatic plants

1.8

Roots in g r o w t h posit ion

2.0

Black gelatinous, ironrich m u d

More o r less undisturbed Bagshot sands

Fig. 18. Typical core through the low-energy Huvio-lacustrine delta at Silwood Park, Berkshirc. England. showing the positions of thc lower ( I ) and upper (2) leaf beds in relation t o sediment types. and the position of lcaf horizons associatcd with a high energy influx of sand bctween 1.2and 1.4mdepth.(FromSpicer. 1981).

out detritus from upstream communities (McQueen, 1969) and contributes its own litter to the stream so that in time the composition of the upper plant bed will become similar to that of the lower bed. Progradation of the delta also increases the ratio of the lake perimeter to its surface area. The preservation of organic material increases, and the plant beds may well thicken (Fig. 19). This pattern of assemblage formation and basin infilling has important im-

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ROBERT A. SPICER

Fig. 19. Block diagram showing the development of a binary leaf bed in a lateral lake system. (Modified from Spicer and Grrer. 1986).

plications for the understanding and reconstruction of ancient communities. Vertical sections through the infilled lake parallel to the direction of infilling will reveal two distinct beds (Fig. 20), differing in species content, which reflect the composition of spatially separated source communities and the successional development of hydrosere vegetation. In this case vertical changes in species composition between assemblages does not reflect changes in vegetation with time (the usual interpretation) but contemporaneous spatial distributions. Temporal developments are reflected in lateral changes in species composition within single beds. 2. High-energy Systems The formation of plant megafossil assemblages in fluvio-lacustrine deltas fed by high-energy streams was investigated by Spicer and Wolfe (1987). Here quite a different pattern of plant deposition was seen, but one equally compatible with the Jopling model as that noted in the Silwood study. Six deltas were studied, each at the mouth of separate drainages surrounding Trinity Lake, northern California. The bulk of the deltaic sediments was deposited during floods in 1964 and 1973 and consisted of gravels, sands and silts. Typically, plant material was deposited throughout the deltaic sediments, but was often concentrated in the toesets and foresets. Hydraulic sorting was in evidence, and material with the highest setting velocities (seeds and fruits) was well represented in the foresets, whereas plant parts with low settling velocities (e.g. moss fragments) were found in bottomsets. Toeset deposition was also enhanced by collapse of foreset slopes. In this situation the inorganic sediment had much higher settling velocities than that of the plant debris, and the flow velocities that transported the sands and gravels to the lake also maintained most of the plant material in suspension until it had passed over the top of the delta slope and had fallen into the zones of mixing and backflow (Fig. 21). Although the binary plant bed pattern seen in the Silwood study was not formed, and consequently in-

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a Direction of infilling P

N,>>NL

Upper leaf bed

N,>>

ND

Lower leaf bed

b

Lower leaf bed

Fig. 20. (a) Diagrammatic representation of variations in species composition between upper and lower leaf beds during lake infilling-N,, is the number of leaves derived from distant sources and N, is the number of leaves derived from local sources; (b) as infilling progresses the difference in species composition, represented as a distance measure D, decreases as the litter from distant sources is filtered and diluted out by the developing delta community. (From Spicer, 198 I ).

formation on the spatial distribution of taxa in the source vegetation was not preserved, the overall composition of the plant debris accurately reflected the overall aspect of vegetation within the drainage area. Although hydraulic sorting concentrated certain elements in different parts of the vertical delta profile, sampling of all parts of the delta complex yielded examples of all types of plant organs, including woody roots of the stream side and possibly forest taxa. During the violent weather that often accompanies flood events, fresh materials may be stripped from plants and incorporated into the floodwaters. At the same time, stream-bank erosion introduces large quantities of forest-floor litter and undercuts whole trees which eventually can also contribute to the potential fossil assemblage (Spicer, 1980). The flood transport of fresh material, forest-floor litter and plant debris already in the river system means that when the plant debris arrives at the delta (or other depositional site) it will be in a variety of states of saturation and will exhibit a larger than usual range of settling velocities. This precludes any particle-by-particle predictions of assemblage build-up, but useful generalizations can be made on a statistical population basis, as witnessed by the observed hydraulic sorting of moss fragments and seeds. The six drainages studied a t Trinity Lake (Spicer and Wolfe, 1987) supported a variety of vegetational communities. Three drainages (Mule, Strope,

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ROBERT A. SPICER

Lake

c

- -

VPl I,,!

11.,,11~,,.,111111)

It, 1.O m diamater) trunks were snapped transversely (Fig. 31a), and showed other signs of traumatic injury (Fig. 31b), buried adjacent to them in the blast deposits were delicate structures such as intact

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ROBERT A. SPICER

Fig. 31. (a) Traumatic blast injury to a mature Pseudorsuga tree approximately 8 km to the north of MSH; (b) volcaniclastics blast-impacted into a tree 8 km from MSH-the scale coin is 24 mm in diameter; (c) female cone of Pseudorsugu, found adjacent to the log in a and lying next to blast-pulverised wood.

female cones of Pseudotsuga menziesii complete with exserted bracts (Fig. 31c). The structure of the blast cloud was complex, and in many respects it acted as a dense fluid. Many of the lighter, more easily transported, plant parts were buoyed up in the cloud and suffered only minor damage. During the post-eruption re-establishment of drainage systems, reworking of this material into sediment traps potentially may provide a moderately complete picture of the pre-eruption vegetation.

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Fig. 32. (a) Vertical aerial photograph of El Chichon taken in 1975 showing the mozaic of natural paratropical rainforest on the summit and slopes, and the cultivated areas in the Rio Magdelena valley (the Rio Magdelena is in the bottom right quadrant of the photograph); (b) lateral lakes, arrowed, along the debris-filled Rio Magdelena as it appeared in March 1984;; (c) El Chichon crater (almost 1 km in diameter), corresponding to the central peak shown in a, and the Rio Magdelena valley, March 1984.

2. El Chichbn The eruptions of El Chichbn, Chiapas, southern Mexico (Fig. 32a), between 28 March and 4 April 1982, produced no lateral blast but provided a suite of depositional environments that in many ways were similar to those seen at MSH.

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The first eruption explosively removed the summit cone that was clothed in paratropical rainforest (sensu Wolfe, 1979). A column of ash and sulphurous aerosol rose to a height of 16.8 km and produced several centimetres of airfall ash over a wide area of southern Mexico. Eventual column collapse produced pryoclastic flows and surges that devastated about 154 km2 of cocoa (Theobrorna cacoa) and coffee (Cogea)plantations, admixed with predominantly second-growth paratropical rainforest immediately around the volcano. Areas of cultivated beans and corn existed near populated areas. Further intermittent activity culminated in two major explosive eruptions on 3 April and 4 April. Detailed descriptions of the eruptive activity are given in Varekamp er al. (1982), SEAN Bulletin (1982), Duffield et al. (1984) and Sigurdsson et al. ( I 985). Apart from the lack of lateral blast, the El Chichon eruptions differ from the 18 May 1980 eruption of MSH in several other respects. Column collapse inundated standing vegetation with hot surge pyroclastics which were mainly channelled along existing drainages radiating from the cone. As a consequence of this, much of the plant material in these drainages was exposed to intense heat ( > 300°C) for periods ranging from days to months while the flows cooled. Entombment within the flows, some of which near the base of the cone were over 20 m thick, prevented air from reaching the organics, and as a result charcoalification occurred either superficially (Fig. 33a) or, in the cases of some large logs, throughout (Fig. 33b), so preserving external morphology and cellular structure in exquisite detail. Although less violent than the lateral blast at MSH, the pyroclastic surges stripped or buried proximal vegetation at El Chichon. At the periphery of surge damage (approximately at a radius of 6 km but dependent on local topography) the surge cloud convectively rose to kill only the canopy trees by heat and mechanical removal of leaves and branches. B. DEBRIS FLOWS

At MSH, blast-ejected material and gravity-slumped mountainside, coupled with groundwater, glacial meltwater and condensed steam, produced a 16-km long debris flow (a lahar) that filled the approximately 1-km wide North Toutle river valley to an average depth of 45 m. The advance of the debris flow scoured topsoil and vegetation from the valley sides and, because the organic material was less dense than the inorganic, it formed an extensive organic “plug” at the leading edge of the flow (Fig. 34a). Over 90% by volume of this wedge was soil and pulverized wood supporting transported whole trees, many of which were upright. Had the US Corps of Engineers not destroyed this deposit in a vain attempt to dam the valley against further mud flows (the dam was overwhelmed), this organic deposit may have been buried by subsequent downstream sediment transport and mud-flows. The

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Fig. 33. (a) Tree base charred by hot pyroclastic flows 6 km from the vent of El Chichon; (b) charcoalified transported log in El Chichon pyroclastic flows. Charcoalification renders plant material inert and thus increases the preservation potential.

advancing debris flow pushed the river waters ahead of it and this water, together with dewatering of the debris flow, produced extensive flooding, sediment transport, and deposition throughout the Toutle drainage (Janda et al., 1981; Pierson, 1985). Downstream of the debris flow, hyperconcentrated stream flow scoured and buried valley-bottom vegetation. Commonly, soil horizons remained intact and flexible saplings remained in situ but with leaves and branches stripped and the trunks abraded to form sharp apical points (“bayonets”)

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Fig. 34. (a) Transported trees at the leading edge of the North Toutle River valley debris flow at MSH-some trees were in life position; (b) blast and/or debris flow-transported block of forest floor containing seeds and rhizomes of pre-eruption vegetation acting as an innoculum for colonization of the debris surface. Photograph taken in August 1982.

pointing downstream. In all there were at least three periods of hyperconcentrated stream flow in the Toutle River drainages (Fritz, 1986) and probably there would have been more had the lakes in the area (see below) not been artificially drained to prevent further flooding. A small eruption in March 1982 melted snow in the crater and resulted in additional hyperconcentrated flow in the North Toutle River valley (Waitt et al., 1983). This prolonged intermittent activity following a violent initial eruption is common in

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163

Fig. 35. Hypothetical composite section through sediments deposited by successive hyperconcentrated steam flows. a, pre-event soil horizon; b, basal graded gravel; c, horizontally stratified gravels and sands; d, matrix-supported muddy sediments containing pumice blocks and assorted organic debris. In subsequent events the development of a soil horizon will depend on the duration of the time interval separating events, and similarly the concentration and nature of the organics in d will depend on the degree of vegetation recovery. (Based on Fritz, 1986)

explosive vulcanism and potentially provides additional sediments for sealing deposits formed by the initial, and earlier subsequent, events. The lack of a glaciated summit at El Chichon meant that during the eruptions relatively little water was available to form lahars. However, pyroclastic flows dammed the Rio Magdalena for a period of approximately three months until the ponded water, forming a lake over 4 km in length, overtopped the dam. Rapid downcutting by the escaping water eroded the dam in a matter of minutes and a flood of hyperconcentrated stream flow, heated by passage through the still-hot pyroclastics, surged down the river valley. Typical deposits produced by a single hyperconcentrated stream flow event consist of a basal graded, closed-framework gravel overlain by a horizontally stratified gravel and sand (Fig. 35). Capping the unit typically there is a matrix-supported muddy mixture containing large pumice boulders and most of the transported organic debris (Fritz, 1986; Harrison and Fritz, 1982). Not only was this type of deposit seen at MSH, but it was also

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ROBERT A. SPICER

Fig. 36. (a) The fern Pityrogramma calamelanos regenerating from buried and exhumed rhizomes on the slopes of El Chichbn in March 1984; (b) deposits in the Rio Magdelena River valley resulting from the “Agua Caliente” hyperconcentrated stream flow produced by the breakout of the eruption-ponded Magdelena Lake. Cocoa (Theobroma) leaves can be seen protruding from the deposits at the base of the horizontallystratified gravels (cf Fig. 35).

observed at Nevado del Ruiz and occurs in many Tertiary deposits (Fritz, 1986). At El Chichbn a similar type of deposit was formed by failure of the Rio Magdalena pyroclastic dam. In this instance the deposits contained coriaceous cocoa leaves (Fig. 36b). Fritz and Harrison (1985) noted that 5-15% of the transported tree population remained upright during transport, while the remainder were deposited as horizontal logs, often orientated by the flow. The main factor determining upright stability is the trunk length/root diameter ratio. Trees with a ratio of 1 or less are upright stable. Karowe and Jefferson (1987) reported the transport at MSH of a “rafted island” of forested land measuring 10 m by 20 m, and pointed out that unless sufficient exposure is available in fossil situations, such rafts could be confused with in situ forest growth. Differentiating transported from in situ trees is clearly essential for accurate interpretation of ancient communities. Fritz (1986) noted that at MSH even transported trees had small hair roots intact, but larger roots tended to be rigid and were often broken off. In addition the root masses contained boulders and cobbles, so the presence of such features in the fossil record is poor evidence for in-place preservation. While the centre of channels rarely contained anything but transported debris, channel margin and overbank

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I65

deposits yielded mixed transported and in situ trees (but see Karowe and Jefferson (1987)). Growing riparian trees were commonly killed by the heat of the flows (- 70°C) even though they were buried by a metre or less of sediment. Thus their bases and abscissed aerial parts may eventually be preserved. Channel margins therefore provide a mixed assemblage potentially representing several communities and, if local topography is pronounced, several zones of microclimates. Fritz (1986) suggested that if the proportion of upright to prone trees is greater than 15% some, or all, of the assemblage may be in place. However, this must be coupled with a detailed analysis of the position of the deposit with respect to the channel itself, and of associated paleosols (if any). Another factor to be taken into consideration when interpreting fossil tree assemblages is evidence for post-burial continuation of growth, such as the development of abnormal growth bulges and reaction wood (Karowe and Jefferson, 1987). Such features would not be expected to any significant extent in transported trees. Repeated hyperconcentrated stream flow events would rapidly build up substantial thicknesses of superimposed units such as the one described above, each with an upper layer containing organic debris (Fig. 35). The nature of this organic assemblage depends on the amount of material available for burial. Thick units with tree bases and logs are to be expected in deposits produced by the initial eruption, but subsequent deposits may be more sparse, depending on the time intervals between events in relation to the rate of vegetation recovery. Each event may also preserve the vegetation (if any) over which it passed, and comparisons of the buried in situ (as compared to transported) debris may provide data critical to differentiating spatial differences in communities and the dynamics of post-disturbance recovery. Not all debris flows passing through vegetated terrain preserve plant material. The eruption of Nevado del Ruiz in 1985 produced no lateral blast, but collapse of the eruptive column led to pyroclastic flows and melting of glacial ice (Fritz, 1986). The resulting mud and debris flows travelled down drainages for more than 60 km over a vertical distance of 5000 m. The high velocity of these flows apparently pulverized trees that were stripped from valley sides. Deposits some 30 m in thickness could be seen 40 km from the vent, but in the more distal regions the flows spread out as thin (< 1.Om thick) sheets. These distal deposits did contain some transported trees as well as wood splinters, leaf debris and pollen (Fritz, 1986), and smelled of methane and decaying plant matter shortly after deposition. A characteristic of vegetation in volcanic terrains, particularly that in valley bottoms, is that it is prone to repeated disturbance. Even if it were to be demonstrated that superimposed fossil stump fields (e.g. Jefferson, 1982) represented in-place fossil forests, the repeated disturbance is likely to render suspect climatic or ecological inferences based on tree spacing or growth-ring data. Minor influxes of sediment, particularly if hot, are sufficient to elimin-

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ROBERT A. SPICER

ate crops of seedlings and may be difficult to detect after root disruption. Certainly such disturbed “fossil forests” should not be taken as representing more regional “steady-state’’ conditions or as being typical of undisturbed forests (cf. Creber and Chaloner, 1984, 1985; Francis, 1986) without first determining the frequency of disturbance. C. PRESERVATION IN AIR-FALL TEPHRA

Air-fall tephra composed of pumice pieces several centimetres in diameter down to extremely fine ash particles affects a much wider area around a volcano than blast, lahars or pyroclastic flows. The grain size of air-fall tephra generally decreases with increasing distance from the vent and its distribution is dependent on prevailing wind conditions and rainfall. Ash layers are common in many fossil deposits and are used frequently for correlation purposes. However, the extents to which ash fall affects the standing vegetation, and its role in preservation, are discussed only rarely. Studies at MSH showed that several centimetres of air-fall ash at ambient temperatures has little effect on standing vegetation. Shoots of evergreen conifers could be seen growing through consolidated ash even when it was compacted between needles and had remained in place for several months. Ground cover was similarly little affected except when it was completely buried under several centimetres of ash. Indeed there is some evidence from the effects on agriculture that decimation of the insect population and the supply of micronutrients actually increases yield where ash fall is light. In areas distal from a vent, ash-fall alone is unlikely to bring about substantial vegetational disturbance or changes in community composition unless ashfall is great and/or repeated at great frequency (several times a growing season for several consecutive years). The concentration of organic debris within air-fall ash (as distinct from blast deposits) in areas proximal to MSH was in most part very low (Waitt and Dzurisin, 1981) (Fig. 37). Presumably this was because the energy of the lateral blast transported the debris to more distal regions. Ash layers within alpine lakes in the Pacific Northwest of North America are commonly encountered (e.g. Dunwiddie, 1986) and may play a role in the preservation of lake-bottom organics. Not all ash falls dry. The thermal and convective energy together with water vapour released by an eruption frequently produce intense rainstorms, and as ash particles fall through the wet atmosphere they accrete into spherical lapilli. The grain size, chemistry and atmospheric conditions all combine to form a variety of ash-fall deposits that preserve various elements of vegetation in different ways. This aspect of taphonomy is little studied as yet but the following example shows the type of information that might be recovered.

FORMATION A N D INTERPRETATION OF PLANT FOSSIL ASSEMBLAGES AIRFALL

SANDV SILT, LAPILLI

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PCCRETlONARi LAPlLLl UNIT

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PEBBLE GRAVEL, SAND, SCATTERED WOOD

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S O I L / FOREST FLOOR

Fig. 37. Composite section of blast and air-fall deposits at MSH.

At El Chichon the multiple eruptions produced a sequence of deposits that contain considerable information about the structure of the standing vegetation. In 1984, Burnham and Spicer (1986) excavated a series of I-m2 plots at various distances from the crater, and noted the occurrence and nature of plant remains in the context of the 1982 ash stratigraphy. Areas where all the vegetation was killed were studied as well as areas in which the vegetation received only a few centimetres of ash fall. A typical section is shown in Fig. 38. All the ash sequences rest upon the pre-eruption soil horizon, and the initial upward-fining pyroclastic deposits produced by the initial (28 March) eruption (approximately equivalent to the A1 airfall deposits of Sigurdson et al., ( 1 984)) preserved the autochthonous forest-floor litter together with the remains of ground-cover plants. Even relatively delicate elements such as Selaginella spp. were preserved. This unit was often capped by a crystalline tuff which in turn was overlain by very fine ash deposits in which leaves of Theobroma were preserved both as compressed intact material and as finely detailed impressions. Typically, the fine ash coated both leaf surfaces, and the early formation of impressions means that even if all the organic material eventually decayed, a record of the leaves would still exist. This layer (equivalent to the Sigurdsson et al. (1984) A2 ash of the 3 April eruption) was barren in areas that were not planted with Theobroma. Overlying this ash layer were varying amounts (depending on proximity and exposure to the vent) of ash and pumice, together with occasional organic fragments and airfall lapilli. These were interpreted to be the result of the final phase of eruptive activity. The basal litter layer reflected the herbaceous ground cover, the subcanopy, the canopy and occasional epiphytes. Although flowers were rare,

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Fig. 38. Section through air-fall deposits produced by the 1982 eruptions of El Chichon. a. pre-eruption soil horizon; b, preserved pre-eruption litter and ground cover vegetation; c. fining upward air-fall ash produced by the eruption on 28 March; d, crystalline tuff; e. fine ash with leaf impressions of Theobroma abscised as the result of ash-induced light attenuation on 28 March and air fall from eruption on 3 April; g, ash from the final phase of eruptive activity; h. recovery vegetation. Thickness of the sequence is variable, but typically not more than 1.0 m (based on Burnham and Spicer, 1986).

fruits and seeds were frequently encountered. The second plant layer, which almost exclusively consisted of Theobroma leaves (Fig. 39a), was interpreted to have resulted from predisposition to abscission induced by light attenuation from ash produced by the initial eruption. Leaf fall occurred under the weight of wet ash deposited on 3 April. Successive eruptions over a short period of time can therefore produce sequences of overlying plant assemblages that represent vertical structure within the vegetation and not, as one might assume, changes in vegetation with time. Scattered throughout the air-fall ash and surge deposits at El Chichon were isolated charcolified or scorched plant fragments. Exposure to high temperatures, even briefly and before charcoalification can take place, effectively sterilizes the plant material, and this, together with rapid burial, enhances the preservation potential. D. LATERAL LAKES I N VOLCANIC TERRAINS

Mud and debris flows initially choke drainage systems that radiate out from vents. As the flows pass the mouths of tributary valleys, volcaniclastic dams are formed. These dams, some of which in the case of MSH were over 40 m high, cause ponding of tributary streams and as a result a series of lateral

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Fig. 39. (a) Impressions of Theobroma leaves in air-fall ash from the eruption of El Chichbn on 3 April (layers e in Fig. 38); (b) colonization of ash surfaces by climbers at El Chichbn in March 1982. Climbers in the sub-canopy environments survived at the margins of the surge devastated areas whereas canopy trees were killed by the hot convectively rising surge cloud.

lakes form (Figs 27, 30b, 40a,b). The size and longevity of a lake depends on the size of valley dammed, the height and mechanical properties of the dam, and the rate of sediment input into the lakes. Stream inflow eventually leads to overtopping of the debris dam and erosion of the dam itself. The degree of erosion will depend on the mechanical properties of the dam, and although many lakes will be entirely drained, many will not. The pre-1980 Spirit Lake was an example of a “permanent” lateral lake formed by an earlier eruption,

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Fig. 40. (a) A large delta fan developing in Coldwater lake in August 1984-MSH is in the distance; (b) log debris in south Coldwater valley in August 1980. Similar log jams existed in Coldwater lake before they were recovered for timber, and would normally form a major component of basal post-eruption lake deposits.

and the sediments of Spirit Lake are likely to contain a detailed record of multiple phases of vegetation destruction and recovery. Streams flowing in to these lakes rework unconsolidated volcaniclasts, together with the remains of the pre-eruption vegetation (including large logs (Fig. 40b)), into the newly-formed lakes, and fluvio-lacustrine deltas quickly develop (Fig. 40a). At El Chichhn, lateral lakes formed along the side of the Rio Magdalena valley (Fig. 32b) but were drowned by the ponded river. The

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deltas continued to build out into the newly formed Rio Magdelena Lake and when it drained they were exposed for study (Fig. 16b). Observations on these deltas showed that initially the rate of volcaniclastic input is high and plant debris may be present only in very low concentrations. Nevertheless, as weathering forms surface crusts on the exposed ash and drainage systems reestablish themselves, the rate of inorganic sediment supply is likely to fall, grain size will decrease, and the concentration and preservation potential of litter derived from recovery vegetation is likely to increase. As plants recolonize the devastated area, their litter (including pollen) becomes incorporated into the sediments in a similar manner to that already described for non-volcanic settings. Because of the relatively rapid sedimentation rates and the progressive nature of their development, fluviolacustrine deltas in post-eruption lateral lakes potentially provide a detailed record of spatial and temporal relationships of plants during the vegetation recovery. The lake sediments themselves are likely to overlie air-fall volcaniclastics and/or mud and debris flow material containing the remains of pre-eruption vegetation, and this in turn may overlie pre-eruption soil and litter horizons. The lake sediments will mostly be finely stratified fine-grained volcaniclastics blown or washed in from the surrounding valley slopes. Immediately following the initial 1980 eruption the trophic structure of existing lakes in the MSH area was profoundly altered and many appeared to be dominated by micro-organisms typical of anoxic waters (Larsen and Geiger, 1982; Wissmar et al., 1982). Spirit Lake, for example, suffered a 22fold increase in alkalinity, enriched metal concentrations, and an increase in phenolic compounds derived from leaching and partial pyrolysis of organic debris. In spite of the profound limnological disorder, Larsen and Geiger ( 1 982) found I3 species of diatoms in Spirit Lake during August 1980, indicating that recovery was underway. The post-eruption chemistry of all the lakes in the MSH area depended strongly on their positions relative to blast trajectory, ash falls, lahars and pyroclastic flows. By 1984 abundant silica supply and nutrients derived from the weathering of fresh ash had produced eutrophic conditions, and abundant diatom and chrysophyte populations reflected individual lake chemistries (Smith and White, 1985). In Spirit Lake high sodium concentrations were associated with the occurrence of Cyclotella meneghiniana Kutzing, a diatom normally found in slightly saline waters. Fungi typical of those saprophytic on decaying wood were also found in abundance. Diatom frustules and, to a lesser extent, chrysophyte statocysts, often comprise a major portion of lake sediments and may lead to equisite preservation of terrestrially-derived plant litter. Moreover, the composition of the diatom and chrysophyte populations reflects lake chemistries which, as Ferguson (1985) pointed out, play an important role in determining speciesdependent relative degradation rates in leaf litter.

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The post-eruption high rates of sedimentation and abundant supply of mineralizing fluids within volcanic terrains provide the potential for recording in detail vegetation changes associated with severe ecological disturbance. The massive disruption of vegetation proximal to an explosive volcanic event means that large quantities of diverse plant organs are introduced rapidly into sedimentary environments, often with their preservation potential enhanced by heat treatment. Although the energy of the eruption in many cases obscures the evidence for connection between organs by widely distributing parts of the same plant, the burial of pre-eruption soil and litter horizons by air-fall ash, or pyroclastic flows and surges, preserves autochthonous associations and even more or less whole plants. The suite of assemblages produced during eruptive events therefore may provide a good overall sample of the community mosaic as it existed at the time of the eruption. It follows from this, however, that in order to reconstruct the pre-eruption vegetation in any reliable way, several contemporaneous deposits must be examined, and their positions relative to the vent must be determined as accurately as possible. Vegetation preserved during an eruption may or may not be in a climax state. Periodic eruptions disturb communities to a greater or lesser degree (depending on the nature of the vegetation, aspect in relation to the dynamics of the eruption, distance from the vent, etc.), and reset seral development to an earlier stage in the succession or disrupt normal seral stages by selectively removing component taxa. Volcanic disturbance, although similar to disturbance, say, on a “normal” floodplain, often has unique characteristics because, for example, edaphic conditions are changed with altered drainage and chemistry. Nevertheless, assemblages preserved in volcanic terrains can provide data critical to understanding ancient vegetation dynamics. A significant body of literature exists on post-eruption vegetation recovery (e.g. Adams and Adams, 1981; Spicer et al., 1985; Eggler, 1948, 1959, 1963; Halpern and Harman, 1983; Hendrix, 1981; Gadow, 1930; Smathers and Mueller-Dombois, 1974; Manko, 1975), but few studies have been carried out on plant succession in relation to the potential fossil record. As an example of patterns of regeneration that are likely to have different palaeobotanical signals, I shall consider events at MSH and El Chichon and speculate on their possible fossil records. The mixed coniferous forest that formed much of the pre-1980 vegetation in the MSH area had suffered no volcanic disturbance since the eruptions of 1857, and even then the only regions severely affected by those eruptions were probably within 5 km of the vent. Although some logging operations had been carried out, much of the area around Spirit Lake was protected to a degree from logging within the Gifford Pinchot National Forest. Aspects of

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the vegetation are documented in Adams and Adams (1981) and Saint John (1 976). In addition, extensive aerial photograph coverage exists. Recovery within the blast area has depended to a large extent on the degree of disturbance suffered and the thickness of sediments deposited. Within a few months of the 1980 eruption, isolated wind-dispersed angiosperm species, notably composites, had begun to grow even on deep pyroclastics within a few kilometres of the crater. However, the most abundant higher plant, at least in terms of area covered, colonizing exposed ash fields and valley bottoms, was Equisetum regenerating from fragmented and blasttransported rhizomes. In my experience gametophytes and young sporophytes were absent. Ferns were rare and isolated. On slopes where the soil remained in place but covered by only several centimetres of ash, typical understorey and post-disturbance (fire/logging) taxa grew in abundance (e.g. Epilohium, Equisetum, Cirsium and a few grasses). By 1982 these slopes also supported 2-3-m high bushes of several species of Rubus (salmonberry, blackberry) and Sambucus. On the North Toutle valley debris flow, several more or less permanent ponds formed and within 2 years had begun to support marginal communities of Typha. Carex and Juncus. In places, large pieces (2-3-m diameter) of blast- and flow-transported pre-eruption forest floor could be seen supporting diverse communities that had regenerated from the contained seed and rhizome bank (Fig. 34b), and thus acted as inocula. By 1984 large areas of the flow were being colonized by Lupinus. Towards the margins of the blast zone in the Green River valley, mature riparian Platanus trees survived blast and heat-kill largely because at the time of eruption they were still in bud. The leafless branches offered little obstruction to the blast and therefore remained largely undamaged, while bud scales limited heat damage to the young leaves. Similarly, understorey angiosperms, including climbers, fared better than the canopy-forming conifers. Recovery studies lower in the Toutle drainage have been hampered by artificial reseeding with grass and Alnus, but it is clear that the initial phases of recovery would naturally be dominated by Equisetum (by rhizome regeneration) by a variety of angiosperms from in situ or wind-transported seeds, and by fortuitous survival because of the seasonal timing of the eruption. In contrast to the several metres of growth exhibited by some woody angiosperm taxa, naturally regenerating conifers were only several centimetres high by 1984. Clearly, for some time to come naturally regenerated vegetation would be likely to be dominated by angiosperms and mark a complete change from the climax conifer forest. Although angiosperm taxa are more diverse in marginal aquatic (and therefore depositional environmental) settings, in the regional coniferous forest of the Pacific Northwest conifers are well represented in depositional environments not intimately associated with vulcanism (e.g. Dunwiddie, 1987) and would be expected to form a significant proportion of both pollen

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and megafossil assemblages derived from climax vegetation. The relative absence of conifers from the early successional stages of post-eruption recovery, however, is likely to give rise to fossil assemblages in which conifers are absent in the megafossil record (except for reworked eruption-emplaced debris) and variously represented in the pollen record. Quite clearly, both pollen and megafossil assemblages must be investigated together. This pattern of recovery also serves as a warning against naively interpreting angiosperm-rich fossil assemblages in volcaniclastics in terms of regional vegetation and palaeoclimate. Vegetation only gives a clear palaeoclimatic signal when it is in equilibrium with the physical environment; a condition most closely approached in the climax condition. It is now clear that assemblages in volcaniclastic sediments must be assumed to represent vegetation that has suffered some degree of disturbance, albeit possibly minor in the case of thin ash horizons in otherwise “normal” sediments. To my knowledge the only cases where this has been expressly recognized are in the studies of the neogene floras of the Pacific Northwest by Taggart and Cross (1980) and Cross and Taggart (1982). Post-eruption recovery studies at El Chichon offer different insights into bias in the fossil record, particularly as regards the effect of climate and the biology of available recovery taxa. The natural climax vegetation around El Chichon consists of angiosperm-dominated paratropical rainforest. Here species diversity is high, the structure of the forest is complex, and in addition to angiosperms a variety of pteridophytes form components of ground and epiphytic cover. Two years after the 1982 eruptions the primary colonizer in severely devastated areas was the fern Pityrogramma calamelanos L. (Link) (Spicer et al., 1985). In contrast to Equisetum at MSH, young sporophytes of Pityrogramma were observed in large numbers even on well-drained pumice fields on the volcano flanks, and in crevasses within 200 km of the crater rim. The most mature sporophytes were those regenerating from ash-buried rhizomes exhumed at the bottom of erosional gulleys (Fig. 36a). Spore dispersal by wind, constant high rainfall ( > 200 cm per year) and relative humidity, allowed gametophyte survival even on well-drained substrates. At the margins of the surge-devastated zone (approximately 6 km from the vent), and closer to the vent along protected valleys, canopy trees were killed but understory elements, particularly climbers, survived and proliferated. Two years after the eruptions, climbers were observed covering and encroaching on the bare ash surface (Fig. 39b). The over-representation of climbers presents a potential problem in the fossil record in that leaves of climbing plants are considered particularly useful in palaeoclimate reconstructions (Wolfe, 1978). Nevertheless, knowing that over-representation occurs goes a long way towards solving the problem. Because preferential climber survival is unlikely to occur to the same

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extent in vegetation disturbed by other agencies, differentiating volcanic disturbance from, for example, that caused by fire, is essential. Where ash fall was relatively thin, woody angiosperms had regenerated either from seed or rootstocks and grown to a height of over 4 m. This rapid regeneration of a wide variety of taxa reflects both the diversity of the original vegetation and the 12-month growing season. By way of contrast, the growing season at MSH is barely 4 months long for many taxa, and correspondingly recovery is much slower. The diversity of angiosperms at El Chichon provided a rich pool of taxa from which a variety of early colonizers could be drawn. Such diversity is not present in the climax vegetation of the MSH area. The main reason for the strong differences between the patterns of recovery at MSH and El Chichon appears to lie in the contrasting biologies present in the taxa of the pre-eruption vegetation. Conifers suffered more damage and were slower to recover than the angiosperms; a situation likely to persist for some time in view of the longer gymnosperm life cycle. If such profound differences in recovery patterns can be seen in just these two contemporaneous examples (and here I have given only the briefest of accounts), the potential for studying even more exotic dynamics in ancient vegetation under radically different climates and composed of extinct taxa, is very exciting. Armed with just some of the insights into assemblage formation in volcanic terrains that studies of this kind provide, major new contributions to ecology and evolutionary studies are possible. The fossil record, with its extended time-scale, offers a unique perspective on this aspect of biology.

XI. PRESERVATION A N D DIAGENESIS The post-burial chemical and physical changes that determine whether or not a plant part will be preserved, and the quality of that preservation, are varied and, as yet, poorly understood. The most common modes of preservation may be categorized for convenience into compression/impressions, duripartic (hard-part) preservation, permineralizations and petrifactions, and casts and moulds (Schopf, 1975), although these categories are not mutually exclusive. A. COMPRESSlON/IMPRESSIONS

In some instances plant material may become coated with a mineral layer (often iron hydroxide/oxide) in aquatic regimes prior to burial (Spicer, 1977). This phenomenon is most noticeable in post-eruption volcanic terrains, because weathering of fresh ash releases large quantities of iron into stream water. Preferential preservation of plant assemblages in iron claystone

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nodules in bentonites yields high-quality impressions (Spicer and Parrish, 1986). The pre-burial formation of mineral coatings not only protects the plant part from abrasion but it may also deter invertebrate feeders. Once buried, plant material is subject to the compaction processes that occur within the sediment as a result of dewatering and loading by addition of new sediment. Decay of cell contents usually takes place within a few days of death or entry into an aquatic environment, and if air is not excluded, cellulose is also rapidly destroyed, even in woody tissue (Rolfe and Brett, 1969). Herbaceous material therefore has to either form a competent impression template, be mineralized, or enter into an anaerobic or disaerobic environment very rapidly in order to be preserved. If early mineralization does not occur and provide support, sediment loading causes the tissues to compress as cell walls collapse. Walton (1936) proposed that in the compaction process there is very little lateral expansion of tissues and distortion is mostly in the vertical plane. This has been largely confirmed by recent experiments (Rex, 1983, 1986; Rex and Chaloner, 1983), but because of internal tissue complexes and resistant surface features on opposing surfaces, the final topography of the compression fossil and its matching impression can be complex, lead to serious misinterpretations of biology, and thus incur taxonomic confusion. B. DURIPARTIC PRESERVATION

The inert qualities of sporopollenin impart a very high preservation potential to pollen and spores which, consequently, are the most abundant evidence of past plant life. However, other plant substances such as cutin and lignin are also highly resistant to decay. When plant material is heated in the total or partial absence of oxygen, volatile compounds are driven off, and if the process is continued to completion, the result is charcoal (fusain) composed entirely of inert carbon. The charcoalification process typically leads to some shrinkage of the tissues but anatomical detail is preserved (Harris 1958; Alvin et al., 1981). Thus charcoalification either by natural fires or by pyroclastic burial during volcanic activity greatly enhance the preservation potential of plant material and produce fossils yielding levels of botanical information which rival those seen in permineralized specimens. C. TISSUE MINERALIZATION

Plant fossils with the greatest amount of botanical information are those preserved anatomically in three dimensions. Apart from charcoalification, this is brought about by early impregnation of tissues by minerals. Plants are most commonly preserved by various forms of silica (chert, opal), calcium/magne-

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sium carbonate, and pyrite, all of which can preserve individual specimens in clastic environments or occur within fossil peats (Scott and Rex, 1985). In many instances organic cell walls remain after the cellular spaces have been filled with minerals. Such specimens are referred to as being permineralized. Where the organic material has been subsequently replaced by mineral matter (either the same as that infilling the cellular spaces or different), the specimen is referred to as a petrifaction. The processes of mineralization can be complex. Although silicification has been thought of as a process of deposition of silica onto cell wall surfaces (Drum, 1968),or organic replacement on a molecule by molecule basis (Correns, 1950; Iler, 1955), the current preferred model is one of infiltration (Schopf, 1975; Leo and Barghorn, 1976; Sigleo, 1978; Jefferson, 1982; Knoll, 1985). A possible model for silicification in volcaniclastics is given in Karowe and Jefferson (1987), but a comprehensive review of the topic is outside the scope of this chapter. Rates of silicification can be extremely rapid as evidenced by the preservation of cell contents (Knoll, 1985). However, in studies at Mount Saint Helens, Karowe and Jefferson (1987) showed that in woods in that particular environment, incipient silicification could be documented after 100 years burial, and that in woods buried for 36,000 years, silica impregnation of cell walls had taken place. An important consideration here is that in spite of the apparent permeability of the lahar sediments, buried wood survives in an unmineralized state long enough for this protracted process to take place. These observations explain the relatively common occurrence of “fossil forests” in volcanic terrains. The origin of carbonate nodules and sheets in coal (coal balls), in which plant material is permineralized, has been controversial for some time. This is because peat environments are generally acid, whereas alkaline conditions are necessary for the precipitation of carbonate. Preservation is variable, depending on when permineralization took place in relation to decay and compaction processes, but often exceptional detail is preserved, such as cell contents (Taylor, 1977), nuclei (Millay and Eggert, 1974), pollen drops (Rothwell, I977), and gametophytes (Brack-Haynes, 1978). By serial sectioning of populations of coal balls, ancient plants may be painstakingly reconstructed (e.g. Rothwell and Warner, 1984), or used for palaeoecological studies (e.g. Phillips et al., 1985). In spite of the palaeobotanical importance of coal balls, hypotheses concerning their formation are varied. Scott and Rex (1985) review the various explanations that have been proposed, and therefore only brief consideration will be given here. The source of carbonate is a particularly vexing problem. Stopes and Watson (1 908) proposed a marine origin and envisioned sea water permeating uncompacted peat as a result of marine transgressions. However, not all coal-ball-bearing coals are overlain by marine units. Mamay and Yochelson (1 962) suggested that breaching of beach barriers separating coal-forming

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swamps from the sea might introduce sufficient carbonate, but this would also mean that transported marine organisms would occur within some or many coal balls and that there would be massive frequent disturbance of the swamp community due to changes in groundwater salinity and pH. Such changes should be detectable in the palynological record if not in that of the megafossils. Coal balls with marine organisms at their core are common, but are not universally found. Infiltration of the peat by non-marine carbonate-rich groundwater is another possibility (Feliciano, 1924; Evans and Amos, 1961; Phillips and DiMichele, 1981; Retallack, 1986), but this does not explain the marine cores of some coal balls. The diverse nature of coal balls means that all the above hypotheses are valid, but not universally. The variety of coal-forming environments also suggests that no single model accounts appropriately for coal-ball formation. However, another scenario, not considered by Scott and Rex (1985), is also possible and could be taphonomically investigated in modern environments. The recognition that many commercial (thick) coals may originally have been ombrogenous (raised) mires would tend to disfavour both the barrierbreach model and groundwater model, particularly for the upper parts of the seams. However, modern raised mires are known to occur on fluvio-marine deltas. As peat accumulation takes place, subsidence is also occurring and the basal parts of the peat may sink below the base of the non-marine groundwater lens into saline groundwater of marine origin. Thus any given portion of the peat will initially form in an acid environment and subside into an alkaline, carbonate-rich environment, without the living mire vegetation experiencing any effects. The relative rates of peat formation and subsidence will control the thickness of peat immersed in the carbonate source, and the degree of compaction that takes place prior to mineralization. If subsidence outstrips mire growth all the peat could be exposed to marine influence, either by immersion in saline groundwater (equivalent to the transgression model), or storm breaching, or both. Pyritization of plant material is common and can preserve fine detail (e.g. Wilkinson, 1984) and clearly can happen very early in the diagenetic history of buried plant matter. It often occurs in marine environments where sulphur, iron, and reducing situations occur together, but as these ingredients are also present in non-marine settings, particularly where organic matter is accumulating, pyritization itself is not diagnostic of any particular depositional environment. D. CASTS AND MOULDS

The infilling of plant cavities with sediment, either before or after some decay has taken place, has the potential to give rise to a three-dimensional cast of

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the cavity morphology which may or may not have been partially compressed prior to sediment hardening. The cavity left in consolidated sediment after decay of a plant part yields a mould that subsequently may be filled either by sediment or mineral growth (or both) to give a cast. Only gross morphological features are preserved and great care is required in interpreting which surface is replicated, and whether that surface is a true indication of the life condition instead of an artefact of decay. Rex (1985) investigated experimentally the infilling of hollow stems and showed that grain size sorting and progressive infilling within such cavities, apart from being dependent on all the usual sedimentological criteria such flow velocity, grain size mix, and orientation of the cavity with respect to flow, can lead to differential compaction and distortion of plant tissues. However, this distortion, although compounding the difficulties of biological interpretation, can also be extremely useful in documenting depositional history and therefore has considerable palaeoecological significance.

XII. APPLICATIONS OF PLANT TAPHONOMY TO THE FOSSIL RECORD The need to understand fossilization processes as an aid to interpreting individual fossils or assemblages has long been recognized. Indeed, the first quantitative taphonomic study was undertaken as long ago as 1924 in order to understand better both the vegetational composition and climate represented by a fossil assemblage (Chaney, 1924). This was closely followed by Walton’s (1936) pioneering work on compressional deformation. In spite of these and other taphonomic exercises, most taphonomic work has been undertaken during the last twenty years or so. The impact of taphonomy on palaeobotany in general is only just being felt. As a crude measure of this impact it is interesting to note that at the 1980 International Organization of Palaeobotany Conference most papers concentrated purely on the botanical aspects of plant fossils, whereas by the 1984 meeting very few papers failed to discuss to some degree the sedimentological environment of individual fossils or assemblages. The applications of plant taphonomy to interpretations of the fossil record are scattered throughout the literature, and while no single palaeobotanical study has been “revolutionized” by taphonomy, many studies have benefited in some way from it. This impact is perhaps best demonstrated by selecting a few studies that reflect the spectrum of scales at which taphonomy can be useful, ranging from an understanding of the conditions of fossilization of individual specimens to interpretations of regional vegetation and climate. These examples have been chosen because they have incorporated references to researched taphonomic principles rather than relying on interpretation based on speculation.

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The work of Rex (1983, 1985, 1986) and Rex and Chaloner (1983) follows from the work of Walton (1936) in trying to understand the processes that give rise to compression fossils. Here experiments have led directly to a reevaluation of the morphology, and therefore taxonomic treatment, of Carboniferous lepidodendrid leaves (Rex, 1983) and glossopterid fructifications (Rex, 1986). In the case of the compression fossil known as Cyperites, compression artefacts, and their influence on the fracture plane of the fossil during its exposure, gave rise to several forms of compression fossils that were very different to the morphology of the leaf in life. By combining the experimental compression of leaf models based on uncompressed permineralized material with observations of compressed leaves of Cyperites sectioned vertically, it was possible to redefine the genus and demonstrate that at least two fundamentally different types of leaves were borne by the lepidodendrids. In the case of the ovulate glossopterid fructifications, similar combinations of experiments and observations of fossils preserved in different ways have shown that permineralized forms represent different taxa to those represented by compression fossils (Rex, 1986). In addition, of the many models suggested for the life morphology of such fossils, only one (the seed-bearing strobilus of Walton (1936)) seems appropriate to explain the features observed in the impressions. Nevertheless, no single uncompressed structure can explain all the observed variations. It follows from this that glossopterids with fructifications of the Scutum type were more diverse than traditionally envisaged. 8. COMMUNITY RECONSTRUCTION

One of the most exciting reconstructions of an ancient community that has been made recently on sound taphonomic principles is that by Gastaldo (1987b), who studied a Carboniferous clastic swamp environment. Mining operations in Alabama exposed extensive bedding surfaces, allowing detailed assemblage analysis to be carried out along a transect from the levee-bound swamp to a channel back-levee margin. In situ tree bases of Lepidophloios, Lepidodendron and Sigillaria were preserved as casts overwhelmed by, and embedded in, 3-m thick crevasse splay deposits. The crevasse splay also capped and sealed the swamp sediments. Litter beds within the splay deposits were also sampled. Interpretation of the sedimentary system was based on analogous Holocene crevasse splay systems (e.g. Gastaldo et al., 1987). Preserved in situ tree bases and preserved swamp litter show that Lepidophloios was the tree most tolerant of waterlogging and comprised almost pure stands in the deep swamp away from the channel. Closer to the channel, where the levee pro-

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vided a degree of topographic relief (and therefore drainage), Lepidophloios was gradationally replaced by Sigillaria. Understorey vegetation increased the diversity. Closer to the crevasse splay breach, remains of calamites and pteridosperm elements increased in abundance while lycophytes were represented only by isolated leaves and rare strobili. Medullosan seed ferns were represented by large ( > 1 m) frond fragments. Whole lyginopterid fronds were found attached to metres of coiled stem, suggesting a Lane habit. Entire crowns of arborescent pteridophytes were also found. The lack of mechanical degradation and the association of fronds and stems suggests that this assemblage was transported minimally prior to burial, and represents the near channel understorey and/or riparian vegetation (cf. Fig. 6) flushed into the swamp by the crevasse. Proximal to the breach itself, the compression flora consisted of fragmented pteridosperm pinnules and pinnae together with numerous Calamites pith casts. In addition to the buried tree bases, prostrate logs, forest-floor litter, and in-washed debris, other litter horizons were interpreted to have been produced by death and crown break-up of the standing lycophytes. Death and crown break-up were probably not simultaneous, however, as two distinct litter horizons are present. This appears somewhat analogous to the sequence of leaf beds produced by volcanic air-fall ash (Burnham and Spicer, 1986). The distribution and degradation patterns of plant debris seen in this Carboniferous crevasse splay system are without doubt similar to that observed in modern sedimentological analogues. This study, in which virtually no biological analogues were invoked, confirms that the plant diversity distribution and structure in Carboniferous swamps was similar to its modern counterpart, in spite of the total dissimilarity of component taxa.

C. RECONSTRUCTING COMMUNITY SUITES AND REGIONAL VEGETATION

The luxury of having extensive bedding surfaces available for study is rare, particularly in natural exposures. Often the extent of an outcrop is insufficient for detailed characterizations of sedimentary environments, and mapping of within-community taxon relationships is impossible. Nevertheless, reconstructions of suites of communities based on detailed facies analysis in sections can be carried out successfully. For example, Cuneo (1983, 1987), working in Argentina, has recognized several communities in a Permian deltaic system. Swamps were dominated by sphenophytes, while slightly higher ground was occupied by two associations; one was composed of glossopterids, ferns and progymnosperms, while the other was composed primarily of ferns and conifers. Glossopterids and conifers occupied the driest floodplain sites (Cuneo, 1987). These kinds of study can be extended to characterize regional vegetation in

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terms of within-community taxon associations and temporal changes in community mosaics. On the North Slope of Alaska, logistic constraints and natural exposures precluded the type of work undertaken by Gastaldo (1987b); nevertheless, by examining a wide range of sedimentary facies over a wide area, the Cretaceous arctic vegetation has been characterized at the community level (Spicer and Parrish, 1986; Spicer, 1987). The pre-angiosperm late Early Cretaceous vegetation of the Corwin Delta complex of the North Slope, Alaska, consisted of riparian and overbank communities in which Podozamites and Ginkgo trees dominated, with Sphenobaiera as a subordinate component somewhat removed from the river margin (Spicer, 1987). Evidence for this is the ubiquitous occurrence of leaf and shoot litter belonging to these taxa in overbank and channel deposits. The conifers Arthrotaxopsis and Elatocladus were also present. Understorey components consisted primarily of ferns (e.g. Onychiopsis, Sphenopteris and Birisia) and sphenophytes (Equisetites)which are commonly preserved as large frond segments (ferns) or upright infilled axes (Equisetites)in overbank muds. Coal-forming mire communities were probably dominated by conifers (Podozamites is the only foliage form found associated with the coals, and tree bases and prostrate logs have been observed), but these communities were probably of low diversity. Equisetites rhizome systems were consistently found in the palaeosols beneath coals, and were clearly primary colonizers in many situations. Lacustrine margins supported a variety of plants, with taxodiaceous conifers and ginkgophytes predominating. Cycadophytes were limited in diversity compared to lower latitudes. The deciduous Nifssonia is found in near-coastal environments (Nilssonia decursiva), or in shales associated with coals ( N . alaskana). Cycadophytes with finely serrated leaf margins occupied lakeside environments. From spore evidence, lycophytes were also present. Angiosperms first arrived in the North Slope deltaic systems in latest Albian times, and the first angiosperm-rich communities were those along river margins. Plants with leaves belonging to the “platanoid” complex (Pseudoprotophyllum, Pseudoaspidiophyllum, Crednaria and “Platanus”) replaced the riparian Podozamites and ginkgophytes. Although generally supposed to be riparian “weed trees”, the stature of the platanoid leaf producers remains unknown, in that vesseled wood does not occur on the North Slope until the Paleocene (Spicer and Parrish, 1989). By the late Cenomanian, riparian communities were dominated by platanoids, but with a variety of lobed and pinnately veined entire-margined leaves in overbank, lacustrine and interfluve “pond” sediments. The ubiquitous occurrence of taxodiaceous conifer shoots in all facies suggests that in spite of the angiosperm diversity, the regional aspect of the vegetation was coniferous. Angiosperms, cyadophytes, ferns and sphenophytes were subcanopy elements (Spicer, 1987). Deliberate sampling of as wide a range of sedimentary facies as possible allowed taphonomic biases (e.g. over-

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representation of riparian vegetation) to be compensated for (Burnham, 1989) (albeit subjectively), and the physiognomy of the regional vegetation was used as part of an interpretation of the near-polar palaeoclimate (Spicer and Parrish, 1986; Parrish and Spicer, 1988). Taphonomy also played an important role in identifying the deciduous nature of the vegetation. No matter what sedimentological facies were examined, the leaf litter always showed minimal signs of degradation. This was taken to suggest that leaf abscision was synchronous across a wide variety of taxa, and all elements were incorporated into the sediments in a fresh state (Spicer and Parrish, 1986; Spicer, 1987).

D. THE USE OF PLANT FOSSILS IN SEDIMENTOLOGY

Throughout this chapter the structure and composition of inorganic sediment has been used as an aid in interpreting individual plant fossils or assemblages. However, the plant debris is also part of the sedimentary system, and, because its source and hydrodynamic properties are so different to those of the inorganic clasts, it provides important data for improved interpretations of some sedimentary processes and environments. Wnuk and Pfefferkorn’s (1987) study of a Carboniferous swamp compared the observed distributions and orientations of fossil lycopod logs (and other plant debris) with those observed in modern depositional environments. Their sedimentary sequence began with an underclay representing an accretionary floodplain soil which incorporated litter derived from the surrounding lycopod-pteridosperm forest. Episodic flooding built up a succession of horizons, but ordinarily, after the floodwaters receded, root bioturbation tended to destroy the potential assemblages. However, this sequence was terminated by a 5-cm layer of underclay in which plant debris was preserved, suggesting that a final flood event permanently drowned the forest and formed a floodplain lake. Death of the trees followed and crown break-up contributed plant material to the lake sediments. Of particular interest was the unidirectional orientation of lycopod logs in contrast to a random orientation of pteridosperm stems. No known waterrelated process could be invoked to explain the anomalous orientations of the plant parts, particularly as the assemblage was entombed in fine-grained non-volcaniclastic sediment, indicating low-energy deposition. The only model capable of explaining all palaeobotanical and sedimentological features was storm-toppling of the standing lycopods, which fell onto remains of the understorey pteridosperms. Taken in isolation, neither the inorganic sediment record, nor the plant fossil remains, could have been used to interpret the sequence of events that produced the observed sedimentary package.

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XIII. CONCLUSIONS Plant taphonomy is in its infancy, but it is a rapidly expanding field. The complexity of this multidisciplinary subject may give the impression that the diverse processes of assemblage formation prevent proper understanding of ancient plant ecosystems. This attitude is erroneous, but it should be apparent that taphonomy is a double-edged sword. On the one hand taphonomic studies expose inappropriate methodologies, analyses and interpretations, but on the other hand new sampling strategies, techniques of analysis and interpretative methodologies are emerging that allow reconstructions of ancient communities and environments at scales of temporal and spatial resolution previously not thought possible. The infancy of the subject precludes at this time the presentation of an extensive catalogue of examples where taphonomic models have contributed significantly to fossil assemblage interpretation. Nor would such a catalogue be necessarily indicative of the subject’s maturity. No single taphonomic “model” is going to be directly applicable even to a “class” of fossil assemblages, and this “package application” attitude is to be discouraged because it leads to simplistic and potentially inaccurate interpretations. For similar reasons, Miall (1985) criticizes end-member facies model comparison in sedimentological studies of inorganic particles. However, awareness of taphonomic biases is contributing to the interpretation of preservation states, systematics, community reconstructions, palaeoenvironmental studies, and palaeobiogeographic data selection (e.g. Raymond et al., 1985). It is perhaps significant that many examples of the applications of taphonomy to the fossil record have been the result of work undertaken by palaeobotanists with taphonomic experience. Taphonomic studies instil an observational approach in the researcher that forces a closer scrutiny and appreciation of the relationship between organic and inorganic sediments. Attitude and technique are more important than the application of whole models. Models are useful in that they underscore the interaction of processes to give a reasonably consistent sedimentological pattern, but they represent “landmarks” in a continuum of interactions rather than the outcome of an “either/or” process. Traditionally discarded or overlooked fragmental material contains an important taphonomic signal that is essential to our understanding of temporal and spatial relationships within source vegetation. This signal can also help our understanding of sedimentation processes. Putting plant debris in a sedimentological context therefore provides an additional class of sedimentary particles with unique properties. Through enhanced resolution at the community level, palaeoclimate reconstructions are also improved. Indeed, it is clear that corrective measures often have to be taken to compensate for the fact that differential organ transport biases assemblages, and because much of the plant fossil record

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samples disturbed vegetation. Taphonomic studies are helping to identify the most reliable assemblages and sedimentary systems for palaeoclimatological work. They are also highlighting the need for regional studies where a range of depositional environments are represented and from which community heterogeneity, and therefore local bias, can be understood. Plant taphonomy provides the means by which community heterogeneity may be resolved at both the local and regional scales, and thus complements the broad regional “floral” interpretations that abound in the literature. However, taphonomic work has highlighted the need for detailed sedimentological work in conjunction with more traditional palaeobotanical studies. Unfortunately, detailed documentation of the nature, quantity and distribution of plant debris by sedimentologists is practically non-existent in the literature, and until recently it was just as rare to find palaeobotanists recording sedimentological data relevant to their fossil assemblages. This situation is now changing, but it is clear that many of the known, indeed “classical”, plant fossil assemblage sites need to be restudied and re-evaluated in the light of taphonomic research.

ACKNOWLEDGEMENTS I am grateful to the following individuals and agencies for their support of my taphonomic research: Don Peterson, Harry Glicken, and other personnel of the USGS Cascades Volcano Observatory, The Royal Society of London, Servando de la Cruz Reyna, Paul Grant, Robyn Burnham, Peter Crane, David Ferguson, The University of London Central Research Fund, Goldsmiths’ College Research Fund, and the Natural Environment Research Council. I also thank Judith Totman Parrish, Bob Gastaldo, and an anonymous reviewer for constructive criticisms of the manuscript. The photographs in Fig. 26 (a,b) were taken by J. Stewart Lowther, and I am most grateful for permission to reproduce them here.

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Runnegar, B. and Schopf, J. W. (1988). Short Courses in Palaeontology I, pp. 1-167. Palaeontological Society. Saint John, H. The Mountaineer 70,65-77. Sheihing, M. H. (1980). Argumenta Paleobotanica 6, 133-138. Sheihing, M. H. and Pfefferkorn, H. W. (1984). Rev. Paleobot. Palynol. 41,205-240. Schoklitsch, A. (1914). “Uber Schleppkraft und Geischiebebewegung”, pp. 33-39. Engleman, Leipzig. Schumm, S. A. (1981). SEPM Spec. Pub. 31, 19-29. Schopf, J. M. (1975). Rev. Palaeobot. Palynol. 20,27-53. Scott, A. C. (1977). Palaeontology 20,447473. Scott, A. C. and Rex, G. (1985). Philos. Trans. R. SOC.Lond. B311, 123-137. SEAN Bulletin (1982). 7 , 2-6. Shields, A. (1936). Mitteilungen der Preussischen Versuchsanstalt fur Wasserbau und Schlffbau 26, 1-26. Sigleo, A. C. (1978). Science 200, 10541056. Sigurdsson, H., Carey, S. N. and Espindola, J. M. (1 984). J. Volc. Geotherm. Res. 23, 11-37. Smathers, G. A. and Mueller-Dombois, D. (1974). National Park Service, Sci. Monogr. Smiley, C. J. and Rember, W. C. (1985). Div. Am. Ass. Adv. Sci., pp. 95-112. San Francisco. Smith, D. G. (1983). In “Modern and Ancient Fluvial Systems” (J. D. Collinson and J. Lewin, eds), pp. 155-168. Int. Assoc. Sedimentology Spec. Pub. 6. Smith, M. A. and White, M. J. (1985). Arch. Hydrobiol. 104, 345-362. Spackman, W., Cohen, A. D., Given, P. H. and Casagrande, D. J. (1976). “The Comparative Study of the Okefenokee Swamp and Everglades-Mangrove-Swamp Marsh Complex of Southern Florida”. Short Course, Pennsylvania State University. Spicer, R. A. (1975). “The Sorting of Plant Remains in a Recent Depositional Environment’’, PhD Thesis, University of London. Spicer, R. A. (1977). Palaeontology 20,907-912. Spicer, R. A. (1980). In “Biostratigraphy of Fossil Plants” (D. L. Dilcher and T. N. Taylor, eds), pp. 171-183. Dowden Hutchinson and Ross, Stroudsburg, Pa. Spicer, R. A. (1987). Geologisches Jahrbuch Reihe A . 96,265-291. Spicer, R. A. and Greer, A. C. (1986). In “Land Plants”, pp. 1&26. University of Tennessee Department of Geological Sciences Studies in Geology, 15. Spicer, R. A. and Parrish, J. T. (1986). Geology 14,703-706. Spicer, R. A. and Parrish, J. T. (1989). J. Geol. SOC.Lond. (in press). Spicer, R. A. and Thomas, B. A. (1986). Systematics Association Special Volume 31, 1-321. Spicer, R. A. and Thomas, B. A. (1987). In “Alaskan North Slope Geology” (I. Tailleur and P. Weimer, eds), pp. 355-358. SEPM, Bakersfield CA. Spicer, R. A. and Wolfe, J. A. (1987). Paleobiology 13,227-245. Spicer, R. A., Burnham, R.J., Grant, P. and Glicken, H. (1985). Am. Fern J . 75, 1-5. Stopes, M. C. and Watson, D. M. S. (1908). Philos. Trans. R . SOC.Lond. B 200, 167218. Styan, W. B. and Bustin, R. M. (1983). Int. J. Coal Petr. 2, 321-370. Szczepanski, A. (1965). Bull. Acad. Pol. Sci. C1.U 13,215-217. Taggart, R. E. and Cross, A. T. (1980). In “Biostratigraphy of Fossil Plants” (D. L. Dilcher and T. N. Taylor, eds), pp. 185-210. Dowden Hutchinson and Ross, Stroudsburg, PA. Taylor, T. N. (1977). In “Geobotany” (R.C. Romans, ed), pp. 77-93. Plenum, New York.

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Teichmuller, M. and Teichmuller, R. (1982). In “Stach’s Textbook of Coal Petrology”, pp. 5-86. Varekamp, J. C., Luhr, J. F. and Prestegaard, K . L. (1982). J . Volc. Geotherm. Res. 23,39-68. Waitt, R. B. and Dzurisin, D. (1981). U S Geol. Surv. Prof. Pap. 1250,601-616. Waitt, R. B., Jr., Pierson, T. C., MacLeod, N. S., Janda, R. J., Voight, B. and Holcomb, R. T. (1983). Science221, 1394-1396. Walton, J. (1936). Philos. Trans. R . SOC.226, 219-237. Webster, J. R . and Waide, J. B. (1982). Freshwater Biol. 12, 331-343. Wilkinson, H. P. (1984). Tertiary Research 5, 189-198. Williams, A. M . (1963). In “The Enzyme Chemistry of Phenolic Compounds” (J. B. Pridham, ed.), pp. 87-95. Pergamon, Oxford and New York. Wing, S. L. ( I 984). J . Sed. Pet. 54, 52-66. Wing, S. L. (1987). In “Methods and Applications of Plant Paleoecology”, pp. 1-19. Notes for a Short Course, Paleobotanical Section, Botanical Society of America, August, Columbus, Ohio. Winner, W. E. and Casadevall, T. J . (1981) USCeol. Surv. Prof. Pap. 1250,315-322. Wissmar. R . C., Devol. A. H., Nevissi, A. E. and Sedell, J. R. (1982). Science 216, 175-178. Wnuk, C. and Pfefferkorn, H . W. (1987). J . Sed. Pet. 57,212-221. Wolfe, J. A. (1978). Am. Sci. 66.694703. Wolfe, J. A. (1979). U S Ceol. Surv. Prof. 1106, 1-37. Yuretich, R. F., Hickey, L. J., Gregson, B. P. and Hsia, Y. (1984). J. Sed. Pet. 54, 836-852. Yonge, C. H. (1928). Biol. Rev. 3,20-76.

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Primary Productivity in the Shelf Seas of North-West Europe

P. M . HOLLIGAN Plymouth Marine Laboratory. Citadel Hill. Plymouth PL12PB. UK

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Ecological and Physiological Perspectives . . . . . . . . . A . Phytoplankton Distributions . . . . . . . . . . . . B. Control of Phytoplankton Production . . . . . . . . .

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Methodsfor EstimatingPrimary Productivity . . . . . . . . A . Nutrient Budgets . . . . . . . . . . . . . . . . B. Oxygen and Carbon Fluxes . . . . . . . . . . . . C. Biomass Distributions . . . . . . . . . . . . . . D . Primary Productivity Models . . . . . . . . . . . .

212 212 213 215 217

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Environmental Conditions for Phytoplankton Growth in the NW European Shelf Seas . . . . . . . . . . . . . . . . . . . . 217 A . Mixing Processes, Seasonal Stratification . . . . . . . . . 217 B. Light Availability . . . . . . . . . . . . . . . 220 C . Nutrient Availability . . . . . . . . . . . . . . 223 D . Grazing . . . . . . . . . . . . . . . . . . . 225 226 E. Annual Production Cycle. . . . . . . . . . . . . .

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EvaluationofPrimary Productivity Estimates . A . General Considerations . . . . . . B. Mixed Waters . . . . . . . . . . C . Stratified Waters . . . . . . . . . D . Frontal Regions . . . . . . . . . E . Spatial and Temporal Variability . . .

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Introduction

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VII . Conclusions

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Fate of Plant Material within the Shelf Ecosystem

Advances in Botanical Research Vol . 16 ISBN 0-12-005916-9

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Copyright 0 1989 Academic Press Limited All rights of reproduction on any form reserved .

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I. INTRODUCTION The photosynthetic activity of phytoplankton in the surface layers of the oceans accounts for about 93% of organic carbon production in the marine ecosystem (Woodwell et al., 1978), the remainder being due to other types of plants mainly in coastal and estuarine environments. Continental shelf waters are, on average, about three times as productive as open ocean waters, so that they contribute a relatively large proportion of total marine phytoplankton productivity ( 20%) relative to their area. Reliable estimates of phytoplankton productivity are required for assessments of the biological resources of the oceans. Attempts to estimate and compare potential fish yields for particular areas (Jones, 1984; Brander and Dickson, 1984), or to predict the impact of overfishing or hypernutrification (van Bennekom et al., 1975; Ursin and Andersen, 1978) on the marine production cycle, depend on a knowledge of primary production rates and the factors that control these rates. Furthermore, it is now apparent that phytoplankton have a fundamental role in biogeochemical cycling in the oceans through direct involvement in the exchanges of material between the atmosphere, surface waters, deep waters and sediments (Whitefield, 1981). The main relationships of phytoplankton growth to ecological and biogeochemical processes in the sea are summarized in Fig. 1. In general the most useful measurement of phytoplankton productivity is net photosynthetic carbon fixation (i.e. gross photosynthesis minus respiration) per unit sea area over a period of 24 h (or some multiple of whole days). However, there are several basic problems in estimating net production which are given remarkably scant attention in the general literature on the productivity of marine phytoplankton and lead to difficulties in the evaluation of published data. These include: 1. For measurements of carbon assimilation (usually made with I4C as a tracer), uncertainties about the degree to which rates of carbon fixation in the light are representative of net photosynthetic rates (Dring and Jewson, 1982), and about rates of dark respiration (Steemann Nielsen and Hansen, 1959; Raven and Beardall, 1981; Joiris et al., 1982). 2. For oxygen measurements, uncertainties in the photosynthetic assimilation quotients used to convert rates of oxygen exchange (photosynthetic or respiratory) to equivalent carbon values (Williams et al., 1979; Megard et al., 1985). 3. For turbulent waters, uncertainties over vertical mixing coefficients that effectively determine the mean irradiance field, and therefore rates of photosynthesis (Lewis et al., 1984), as well as the depth range over which dark respiration losses must be estimated to give net production for the phytoplankton population as a whole (Sverdrup, 1953). Another important consideration is the relationship between the form of nutrient supply for phytoplankton production and the capacity of the pelagic

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n

Fig. 1. Phytoplankton growth in shelf seas-cological and biogeochemical processes. P, phytoplankton; H, herbivores; C, carnivores; MH, microheterotrophs; DOM, dissolved organic matter; POM, particulate organic matter; VOM, volatile organic matter; Bio, biominerals (opal, calcite). For the sake of clarity, only the more important relationships are shown.

ecosystem to support over an annual time-scale a net export of organic material to deep water, to the sediment, and as fish catches. Growth of the plant cells in surface waters is dependent on a combination of external or “new” inputs of nutrients-mainly resulting from the upward mixing of deep water, but also from terrestrial and atmospheric sources-and of internal or regenerated nutrients released during the biological turnover of material within the euphotic zone (Dugdale and Goering, 1967). The significance of this distinction was examined by Eppley and Peterson (1979), who reached two important conclusions. Firstly, it is the new production of phytoplankton, as opposed to regenerated (or total) production, that represents capacity for the export of organic material from the euphotic zone; secondly in most environments new production is a relatively small proportion (e.g. 30% for a station in the subtropical Atlantic Ocean-Platt and Harrison, 1985) of total annual primary productivity. Although some care needs to be taken in defining the scales over which new and regenerated production is estimated

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(for example, should inorganic nutrients produced by mineralization processes below the seasonal pycnocline and returned to surface waters two or more times within the same year be considered as new nutrient sources?), this general concept has proved invaluable in attempts to assess quantitatively the ecological and biogeochemical implications of phytoplankton growth (Platt and Harrison, 1985). The past two decades have also been a period of rapid progress in physiological investigations on planktonic algae, particularly in relation to the utilization of nutrients and light energy. Much of this work has been based on laboratory experiments with uni-algal cultures, mainly because of the difficulties in interpreting physiological data on heterogeneous natural phytoplankton assemblages. Although the results have added greatly to our knowledge of the various ways in which environmental conditions influence the growth and succession of phytoplankton (Harris, 1984), it has also led to a tendency to use simplified, and often inappropriate, sets of parameters for quantitative descriptions of natural populations (Talling, 1984). Thus, from an ecological standpoint, recent advances in algal physiology have not necessarily added a great deal to our knowledge about rates of primary productivity in the sea. For the NW Europe continental shelf, the generally accepted picture of primary productivity is still based largely on studies carried out more than 20 years ago (Harvey et al., 1935; Steele, 1956; Cushing, 1963). Physical mixing processes in this region are known to exert a fundamental influence on the distribution and abundance of phytoplankton species (Pingree et af.,1978) in a spatial as well as a temporal context. However, except for particular studies such as the FLEX experiment in the North Sea (Radach et al., 1982), few attempts have been made to bring together new ideas on the environment and growth of phytoplankton in a re-evaluation of data on primary productivity. The main objective of this chapter is to summarize present knowledge of phytoplankton distributions and growth in the shelf seas of NW Europe in the context of a broad understanding of phytoplankton ecology, both from experimental laboratory work and from observational studies of other ocean areas. In the sections on the control of phytoplankton production and on methods for estimating primary productivity, the references are largely to the general literature, whereas the remaining sections deal specifically with NW European waters. Such an approach leads to some repetition, but provides a more comprehensive basis for assessing primary productivity in this region.

11. ECOLOGICAL A N D PHYSIOLOGICAL PERSPECTIVES A. PHYTOPLANKTON DISTRIBUTIONS

1. Descriptive Accounts The early studies of P. T. Cleve, H. H. Gran, H. Lohmann, C. H. Ostenfeld

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and others provided much of our basic knowledge of the distributions of larger phytoplankton species in the NE Atlantic Ocean, and this is summarized in the floras of Lebour (1925, 1930) and Schiller (1933, 1937). Subsequent work has been concerned largely with the life histories of diatoms and dinoflagellates, as well as descriptions of the many naked and scalebearing marine flagellates (for references and up-to-date nomenclature see the checklists of Hartley (1986) and Parke and Dixon (1976), and also the account of Helgoland phytoplankton by Drebes (1974)). The ecology of the various flagellate groups is still relatively poorly known, with the exception of a few widespread and easily recognized species such as the prymnesiophytes Phaeocystis pouchetii and Emiliania huxleyi; the investigations by Throndsen (1976), Heimdal and Gaarder (1980, 1981) and Estep et a f .( 1984), although not confined to shelf environments, give some indication of the abundance and variety of these organisms. Furthermore, the presence in shelf waters of numerous photosynthetic prokaryotic and eukaryotic cells, < 2 pm in diameter, has become generally recognized only during the last few years (Joint and Pipe, 1984; Murphy and Haugen, 1985; Fogg, 1986). Another feature of distributional studies is reports of extensions in geographical range for certain species. For example, the large diatom Coscinodiscus waifesii (Boalch and Harbour, 1977) and the bloom-forming dinoflagellate Gyrodinium aureolum (Braarud and Heimdal, 1970) appear to be recent introductions from other parts of the world and are now wellestablished species in European shelf waters. 2. Quantitative Methods The size range of marine phytoplankton extends over at least seven orders of magnitude in terms of cell volume ( < 1 to > 10’ pm3), so that cell concentrations are not a useful measure of total biomass or of relative biomass for individual species. Two approaches are used to overcome this problem, the first based on pigment determinations generally as total chlorophyll a (Strickland and Parsons, 1972), and the second on the conversion of cell counts or chlorophyll to phytoplankton carbon (Strathmann, 1967; Banse, 1977). Although both methods are subject to several sources of potential error, they do give internally consistent measures of spatial and temporal differences in phytoplankton standing crop (Holligan et al., 1984a) as well as information on the contribution of individual taxa (e.g. accessory pigment groupings (Mantoura and Llewellyn, 1983)) or species to the total population. Statistical techniques for deriving phytoplankton carbon from measurements of particulate organic carbon, with the condition that the phytoplankton represent a variable and often minor component of the total carbon, have also been developed (Eppley et al., 1977). An ancillary method for discrete pigment determinations is the use of in vivo fluorometry (Lorenzen, 1966), which provides a continuous record of chlorophyll fluorescence as horizontal (surface) or vertical (depth) profiles

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that can be compared with those for temperature, salinity or other hydrographic properties. Great care must be taken over calibration of the fluorometer records, as fluorescence yields per unit chlorophyll can vary by up to an order of magnitude with changes in physiological state or species composition of the phytoplankton population (Pingree et al., 1982). For studies of large-scale distributional patterns of phytoplankton, use has been made of the colour (pigment) index given by tows of the Continuous Plankton Recorder (CPR) (Robinson, 1970). Some caution must be exercised in the interpretation of CPR data as the mesh size (270 pm) of the collection net will tend not only to select the largest phytoplankton cells but also vary as a result of partial clogging within dense populations. Furthermore, the monthly sampling interval for the routine CPR routes may be too infrequent to resolve some of the main features of phytoplankton succession in temperate waters. Ten years of chlorophyll measurements for March to July in the northern North Sea are compared in Fig. 2 with monthly CPR colour indices over a similar period. Detailed ship studies, such as the 1976 FLEX experiment (Radach et al., 1982), confirm that the duration of the spring diatom bloom is generally less than two weeks. Thus, in the CPR records, the absence of a spring outburst on some years (Fig. 2b) is probably not real but attributable to infrequent sampling, and the apparent decrease in the total abundance of spring phytoplankton (Reid, 1978) may reflect just a decline in numbers of large diatoms which are generally a minor component of the spring bloom. 3. Temporal and Spatial Distributions Through the many observations on species abundance, chlorophyll concentration and the CPR colour index, a consistent picture of annual changes in phytoplankton abundance has been built up. There are marked differences from one type of environment to another (e.g. Robinson et al., 1986), due mainly to the influence of vertical mixing on the availability of light energy and nutrients to the plant cells (see Section 111 for a detailed discussion). The extremes are seasonally stratified waters, which are characterized by surface chlorophyll maxima in the spring and autumn and a subsurface maximum in the summer associated with vertical nutrient gradients in the thermocline (Fig. 3; Holligan and Harbour, 1977), and well-mixed waters with just a midsummer chlorophyll peak extending through the whole water column (e.g. in the Bristol Channel (Joint and Pomroy, 1981)). However, there are still relatively few sets of observations to show the complete seasonal cycle of phytoplankton, so that the CPR data remain the best general source of information for comparing one region to another. For example, the distinction between stratified and mixed waters is well shown by the CPR data for the central North Sea and central Irish Sea respectively (Colebrook, 1979). One feature that has yet to be properly assessed by more absolute sampling methods is the autumn phytoplankton maximum. As

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Fig. 2. Comparison of surface chlorophyll a measurements, 1961-1970 (from Steele and Henderson, 1977) (a) and the CPR pigment index, 1958-1973 (from Reid, 1977) (b) for the northern North Sea. For any particular year the spring bloom, defined as chlorophyll values > 2 mg m -3, appears to last about two weeks (e.g. Radach et al., 1982). The relative chlorophyll levels represented by the contours of CPR pigments are approximately 1.0 : 1.6 : 3.4.

pointed out by Steele (1956), rates of production are very variable at this time of year, and results from the CPR indicate that this is particularly true for regions of intermediate seasonal stratification such as the central North Sea (Reid, 1978). A complementary approach to studies on temporal distributional patterns

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Fig. 3. Annual chlorophyll a (mg m I) distribution at station El in the western English Channel based on two years observation (1975-1976). Adapted from Holligan and Harbour (1977). who give details of sampling methods.

is to consider spatial (horizontal) changes in phytoplankton biomass. A detailed study of this type was carried out by Pingree et al. (1975), who related differences in phytoplankton abundance and species composition to hydrographic properties on a section across a tidal front in the western English Channel. The results showed not only the clear difference between well-mixed and well-stratified waters during the summer, but also the enhanced biological activity in association with the transitional frontal boundary (Fig. 4). The characteristic time- and space-scales of changes in chlorophyll concentrations (Figs 3 and 4) demonstrate the difficulty of adequate sampling in heterogeneous shelf waters. These have now been largely overcome, through the development of continuous sampling techniques, based on the use of pump methods (Pingree et al., 1975), of towed in situ instruments (e.g. Fasham et al., 1983a; Aiken and Bellan, 1986), and of remote sensing techniques (e.g. Holligan et al., 1983a). Another important feature of phytoplankton distributions concerns species succession. Numerous observations on temporal changes in species abundance and dominance confirm the classic pattern for temperate shelf waters of spring and autumn diatom peaks, and a mid-summer dinoflagellate maximum (Smayda, 1980). This pattern reflects changes in the availability of light and inorganic nutrients in the surface layers (Margalef, 1978), and can also be observed in a spatial context during the summer months as the transition from diatom populations in persistently well mixed waters to flagellate populations in seasonally stratified nutrient-depleted waters (Holligan, 1981). Superimposed on fluctuations in the abundance of the two main groups of larger phytoplankton is the development of coccolithophore blooms in early summer (Holligan et al., 1983b), which appear to occupy an

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Stations 3

I

JQb \

! 40c

i It

'i

0

-E

1

f

20

8 n 40

Fig. 4. Distribution of (a) temperature (T),(b) chlorophyll a (mg m-", and (c) nitrate (pM), across a section of the Ushant tidal front in the western English Channel, 2 August 1976. Station 30 (49' 40' N; 04"50' W) is in mixed water closest to land, and Station E5 (49"05' N; 06" 37' W) is in stratified water. From Holligan (1979).

intermediate successional position, and of low-biomass, climax communities dominated by autotrophic cyanobacteria and very small eukaryotic cells (Joint and Pipe, 1984) under conditions of strong surface stability. Patterns of succession are also recognizable at the species level (Maddock et al., 1981; Horwood et al., 1982; Wandschneider, 1983). Few studies of primary productivity in marine waters have included an analysis of phytoplankton species composition. As a result information on morphological (e.g. in relation to palatability for herbivores, sinking rates) and on physiological (biochemicalcomposition, nutrient requirements, capacity for extracellular release of carbon) characteristics is generally not available for evaluating productivity data within ecological or biogeochemical contexts. Furthermore, rather little is known about changes in photosynthe-

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tic properties that accompany shifts in species dominance or the collapse of a bloom. B. CONTROL OF PHYTOPLANKTON PRODUCTION

The effects of light, nutrients and temperature on phytoplankton growth have been extensively studied under laboratory conditions using uni-algal cultures. For natural populations of phytoplankton, light and nutrients rather than temperature are more important in controlling rates of production (Tett and Edwards, 1984), as they represent essential resources which are not always sufficient to support net growth in the water column. Situations of light limitation in the sea are readily identifiable in terms of vertical mixing of surface layers or of high turbidity due to particulate material other than phytoplankton. By contrast, nutrient limitation is more difficult to define, mainly because of the complex adaptive responses shown by phytoplankton populations to changes in the rate or form of nutrient supply. The main conceptual problems concern the distinction between rates of specific growth (biomass-independent) and rates of production (biomassdependent), and the dual effects of herbivory as a cause of mortality and as a source of regenerated nutrients (see King, 1986). Under natural conditions, nutrient limitation of population growth tends to be a transitory state, as cell losses from sinking and grazing, species replacement (succession), and nutrient regeneration lead to the establishment of a new species assemblage with different nutrient requirements that are met by the new conditions of nutrient supply. Marked changes in species composition and total algal biomass can occur over a period of a few days (e.g. Fasham et al., 1983a), reflecting the nutritional versatility of multi-species populations and the rapid rates of cell division and mortality. However, they are not necessarily accompanied by changes in growth rate; indeed, the available evidence suggests that low rates of nutrient supply are correlated with low standing stocks of phytoplankton (Eppley et al., 1979) rather than low growth rates (Goldman et al., 1979). For this reason, nutrient limitation of phytoplankton growth in the sea does not have a precise meaning, and the concept of nutrient control of standing stock or primary productivity is generally more appropriate. Much of the physiological information relevant to an understanding of phytoplankton growth is well described in the publications edited by Morris (1980), Falkowski (1980) and Platt (1981). Here it is sufficient just to emphasize those aspects that are of particular importance for the interpretation of primary productivity data and that have been the focus of more recent research. 1. Light The various problems in measuring photosynthetically active radiation

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(PAR) in aquatic environments are described by Kirk (1983) and Jewson et af. (1984). Values of the scalar irradiance (Eo)are the most useful in relation to rates of photosynthesis. In practical terms, these are most easily derived from vertical attenuation coefficients for scalar irradiance (KO)or for downward irradiance (&) the latter being measured with a cosine collector and giving a reasonable approximation of KO(Kirk, 1983). The scalar irradiance at any depth ( z )is then given by E,(z)

=

E,(0)e-KO'

where Eo(0) is the surface-penetrating photon flux density. Care has to be taken to avoid errors in estimates of Eo(z)for the upper part of the photic zone due to variations in KOor Kd that result from spectral changes in underwater irradiance (Jewson et af., 1984). For a given value of Eo(0)the total amount of PAR available for photosynthesis is approximately inversely proportional to KO(Kirk, 1983). Thus a typical range of 0.08-0.50 m- for KO in continental shelf waters implies a six-fold variation in light availability at any depth for a given value of Eo. Properties that contribute to KO include absorption by water, yellow substances and particulate matter as well as by phytoplankton cells. In general, it is possible to calculate the proportion of light absorbed by phytoplankton from a knowledge of KO,K, (the spectral absorption coefficient for chlorophyll) and chlorophyll concentrations (Morel, 1978) and, therefore, to estimate photosynthetic efficiency and quantum yields for natural populations (Dubinsky et af., 1984; Kishino et af., 1986). However, under conditions of strong scattering by particulate material, KOcannot be assumed to represent the sum of partial attenuation coefficients for absorbing components (Kirk, 1983). In considering the implications of regional variations of the light environment on primary production, it is important to have some method of determining the distribution of KO or Kd with adequate spatial and temporal resolution. There is no easy way of doing this. Light profiles and Secchi disc measurements, the latter being empirically converted to & (Walker, 1980; Preisendorfer, 1986), can only be made during the middle part of the day when the ship is stopped. Transmissometer measurements of beam attenuation coefficients offer the advantage of continuity in horizontal and vertical profiles. However, beam attenuation is the sum of absorbance and scatterance, which are interdependent optical properties of sea water, so that there is no simple relationship between the beam attenuation coefficient and vertical attenuation coefficients for (scalar) irradiance (e.g. Topliss et af., 198& 81). The best hope is offered by remote sensing of ocean colour, but algorithms for deriving the vertical attenuation coefficient (Austin and Petzold, 1981) have yet to be widely tested for NW European waters (Viollier and Sturm, 1984). The utilization of light by phytoplankton in the sea is most simply de-

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scribed (Fig. 5) by two relationships, the classical photosynthesis (Pkirradiance ( I ) curve, and the depth profiles for gross photoSynthesis (P,) and dark respiration (R)which define the compensation (Pg = R) and critical (sipg= SiR) depths. For comparative purposes, photosynthesis and respiration are expressed as biomass-specific rates and RB,with the biomass in units of carbon or chlorophyll. The difference between these rates is the specific net photosynthetic rate P:. When the depth of mixing (Z,) is less than the critical depth (i.e. P: is positive for the surface layer over a complete lightaark cycle or 24-h period), the phytoplankton biomass will increase if there are no losses due to sinking and grazing. Clearly the form of the P-I curve, as defined by the parameters a, P,,, and B (Fig. 5), determines the rate of primary production for any given set of environmental conditions (Eo,KO, Zm). Various methods are used for fitting P-I curves to sets of observational data on carbon assimilation, based on empirical relationships (Platt et al., 1980: Harrison et al., 1985) and on physiological models of light-dependent photosynthetic reactions (Fasham and Platt, 1983; Dubinsky et al., 1984). However, to estimate net production, carbon losses due to dark respiration must be taken into account (Dring and Jewson, 1982). Usually some constant value for R is assumed, but recent evidence suggests that the respiration rate is unlikely to be constant (Raven and Beardall, 1981; Falkowski et al., 1985) either from day to night, or with changes in physiological condition or species composition of the phytoplankton population. Other uncertainties in estimating P: concern the time-scales and quantitative importance of photoadaptation (Marra, 1978; Savidge, 1980; Falkowski, 1983, 1984; Marra et al., 1985; Kana et al., 1985), as well as variability in carbon losses due to photorespiration (Burris, 1980) and related processes leading to the exudation of organic carbon (Fogg, 1983). Despite these complex physiological problems, an analysis of adaptive strategies to different conditions of irradiance does show well-defined and ecologically significant differences between the main algal classes (Richardson et al., 1983). These are best illustrated as different forms of P-I curves (Fig. 6 ) that can be interpreted as responses due to changes in the number and size of the photosynthetic units. Although such interpretations may often be oversimplifications, they do represent a physiological basis for explaining taxonomic traits; for example, diatoms tend to grow well at high photon flux densities compared to other phytoplankton groups, whereas dinoflagellate populations show relatively efficient growth at low irradiances and often exhibit pronounced photoinhibitory responses. 2. Nutrients In temperate and polar seas the highest surface concentrations of the major inorganic nutrients (combined forms of nitrogen, phosphorus and silicon) required for phytoplankton growth are observed in the late winter when assi-

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Fig. 5. Idealized plots to show the relationship for a phytoplankton population between (a) photosynthesis (P) and irradiance (I);and (b) photosynthesis and phytoplankton respiration (R) in a mixed water column under conditions of midday sunlight. Net primary productivity becomes positive when the depth of mixing (thermocline) is less than the critical depth. See text for further details.

milation rates are minimal. The main sources of these nutrients are vertical mixing with nutrient-rich deep water and continuing regeneration from particulate and dissolved organic material. On the continental shelves lateral exchange with oceanic waters across the shelf break and river inputs are also important, the former being generally dominant except close to estuaries or in shallow, enclosed waters (e.g. James and Head, 1972). For oligotrophic ocean waters, rainfall can also be a significant source of nitrogen (Paerl, 1985). With the increase of solar radiation and development of the seasonal pynocline in the spring, there is rapid utilization of these nutrients by diatoms. The particulate organic material formed in the surface waters typically

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I

I/ I

/ PSU no.

/n PSU size

Fig. 6 . Idealized P-1 curves to illustrate (a) genotypic differences between phytoplankton groups, and (b,c) phenotypic responses for high (H) and low (L) irradiances involving changes in the size and number of photosynthetic units (PSU). For further details, see Richardson ei a/. (1983).

has a chemical composition conforming to the Redfield ratios (Redfield, 1958F-C : N : P in the proportions 106 : 16 : 1 by atoms. Although other types of phytoplankton may replace the diatoms if silica becomes depleted, the main declines in phytoplankton biomass and production occur when nitrate and phosphate reach minimal levels. Thereafter, nutrient control on primary productivity is generally thought to be due to low available nitrogen rather than phosphorus (Ryther and Dunstan, 1971), probably because rates of regeneration are somewhat slower for nitrogen, with the result that the ratio of dissolved nitrate to phosphate decreases during the summer (Pingree et al., 1977b). The relationship between nutrients and production in the sea is therefore generally considered in terms of nitrogen availability, although over short (days) and very long (geological) time-scales phosphorus may be more important. As inorganic nutrients are incorporated into organic material, regenerative processes lead to the release into the water of various reduced and organic forms of nitrogen and phosphorus. For nitrogen, these include substances that are readily reassimilated by phytoplankton (ammonium, urea, amino acids) as well as relatively refractory organic compounds. The latter form a substantial proportion of the dissolved organic nitrogen pool, reaching maximum concentrations in mid-summer (Butler et al., 1979), but are probably relatively unimportant for phytoplankton growth except in the most oligotrophic (stable) waters, where rates of primary production are low (Jackson and Williams, 1985). Ammonium and urea are important products of excre-

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tion and ammonification, and probably make up the bulk of the utilizable regenerated nitrogen (Corner and Davies, 1971). Ambient concentrations of nitrate and ammonium in nutrient-depleted, stratified waters are generally close to or below the limits of detection ( 0.1 PM) by standard colorimetric methods. In order to assess the uptake rates of new and regenerated nitrogen, two different approaches have been developed. The first concerns the careful measurement and evaluation of gradients in concentration with respect to rates of physical mixing. This is particularly applicable to estimates of the upward flux of nitrate across the seasonal pycnocline (King and Devol, 1979; Holligan et al., 1984b; King, 1986; Lewis et ul., 1986), but can also be considered in relation to lateral mixing across fronts (Loder er ul. 1982) and along isopycnal surfaces. A new chemiluminescent method for the detection of nitrate in sea water allows a precision of f2 nM and a much improved characterization of nitrate gradients (Garside, 1985), so that the main difficulty is in deriving reliable values for diffusion coefficients. The second approach depends upon the use of I5N as a tracer (Collos and Slawyk, 1980; Dugdale and Wilkerson, 1986) to assess rates of substrate assimilation by natural phytoplankton populations. There are experimental difficulties (Goldman, 1980) concerned with long incubation periods and the addition of relatively high concentrations of carrier substances which are not representative of natural conditions, but these have been largely overcome for eutrophic waters (Dugdale and Wilkerson, 1986). Studies at sea have provided consistent, albeit largely indirect, evidence that the nitrogen requirements of phytoplankton are mainly met by a combination of new nitrate (mixing from deep water) and regenerative ammonium (in siru release by heterotrophs) sources (Eppley et al., 1979; Eppley and Peterson, 1979; Harrison et al., 1983, 1987). Urea also appears to be important in inshore waters (McCarthy, 1972; Turley, 1985, 1986), but for offshore waters the contribution of both urea and amino acids (Fuhrman and Ferguson, 1986; Flynn and Butler, 1986) remains uncertain. The dependence of growth on maintained new inputs of nitrate to balance nitrogen losses from the euphotic zone due to sinking faecal pellets and other particulate matter and to the downward mixing of dissolved organic nitrogen was clearly shown by Eppley and Peterson (1979). Much attention is now being given to evaluating the relationship between ambient nitrate concentrations and the “f-ratio” or ratio of new (nitrate-based) production to total production (Harrison et al., 1987). A much clearer picture has now also emerged from laboratory studies with algal cultures of the relationship between nutrient assimilation and growth in physiological terms. Early growth models based on the classical Monod equation, which related the specific growth rate ( p ) to the external concentration of the limiting nutrient, have now been largely replaced by ones which show growth rates to be dependent on internal nutrient levels (Droop, 1983). The best-known form is the cell quota model: N

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where pm is the maximum growth rate, Q the phytoplankton nutrient content, and Kq the subsistence quota (or minimum nutrient content to maintain viability). The rate of nutrient uptake (u) is considered separately, generally as the hyperbolic Michaelis-Menten relationship:

where u, is the maximum uptake rate, S the external nutrient content and K , the half-saturation constant for nutrient uptake. These equations represent the simplest interpretations of experimental data (mainly from chemostat cultures) but, despite their recognized limitations (Laws and Bannister, 1980; Droop, 1983), they are of ecological significance for several reasons. Only one nutrient is considered limiting at any one time; for nitrogen sources the low ambient concentrations in sea water are compatible with low K , values (e.g. Goldman, 1977); also they imply that growth rates are not necessarily dependent upon external concentrations (Dortch et al., 1485; Collos, 1986). Another important principal to emerge from chemostat studies of steadystate growth concerns the relationships between nutrient supply, standing stock, and dilution (loss) rates. At steady state, the phytoplankton biomass represents the ratio between the nutrient supply rate and the specific growth rate, the latter being set by and therefore equal to the dilution rate. In the sea, grazing mortality is analogous to the dilution rate and acts as a feedback control (excretion) on nutrient supply. Thus, under stable environmental conditions, differences in the rate of nutrient supply to the surface layers will be reflected by comparable differences in phytoplankton standing stock, provided that the growth/grazing rates do not vary greatly (Eppley, 1981). Furthermore, for any given growth rate, standing stock will be linearly proportional to net productivity. Thus observed variations in standing stock are indicative of changes in both nutrient supply and productivity (see King, 1986). There are two outstanding problems concerning the nutrient physiology of natural phytoplankton populations. The first is the interaction of nutrient uptake and growth under conditions of fluctuating nutrient supply (due, for example, to variable mixing across the thermocline, or the vertical migration of zooplankton), which is likely to lead to the condition p # pQ over one or more cell cycles. Such transient nutritional states are discussed by Dugdale (1977) and Droop (1983). The second is the form of nutrient-light interactions, and is particularly pertinent to growth in stratified waters where the main sources for nutrients and light are at the bottom and top of the euphotic

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zone respectively. The opposing vertical gradients in these two properties lead to the potential for interactive effects on phytoplankton growth at all depths over the natural 24-h light-dark cycle. Some recent models treat light and nutrients in a non-synergistic manner (Tett, 1981; Tett et al., 1986), but the physiological complexities are well illustrated by attempts to interpret cell properties (e.g. variance from Redfield ratios for chemical composition) in terms of the combined effects of nutrients and light (Laws and Bannister, 1980; Tett et al., 1985). 3. Temperature From studies with algal cultures, temperature is known to have profound effects on cellular metabolic rates (Li, 1980), and equations for temperature effects based on the Arrhenius formulation for chemical reactions are included in growth models (e.g. Goldman, 1979). Furthermore, different species, as well as different clones of the same species, show marked differences in temperature optima and tolerances for growth. For this reason, conclusions about temperature effects based on laboratory observations must be interpreted with care in an ecological context-for example, an isolate from temperate waters of the coccolithophore Emiliania huxleyi showed little or no growth below 7°C (Paasche, 1968), whereas natural populations of this species are known to occur at temperatures < 0°C (Heimdal, 1983). Fluctuations in sea temperature are less extreme and more gradual than those of air temperature affecting terrestrial environments. At mid-latitudes the annual range of sea surface temperature is typically about IOOC, increasing to about 20°C close to continental land masses. This is sufficient to account for much of the variability in maximum photosynthetic rates both seasonally (Eppley, 1972; Harrison and Platt, 1980) and in relation to latitudinal temperature gradients (Li, 1985). On the other hand, rates of temperature change rarely exceed 1°C per day, so that variations in photosynthetic rates over shorter time-scales are generally considered to be due to other environmental conditions such as light and nutrients. In a spatial context, however, temperature gradients can be relatively steep, with differences in the order of 5510°C horizontally over a few kilometres across surface frontal boundaries, and vertically over a few metres across the seasonal pycnocline in continental shelf waters. In general the species composition of the phytoplankton changes across such temperature gradients, and only in the case of dinoflagellate populations exhibiting die1 vertical migrations across the thermocline (Blasco, 1978) are cells of a particular population exposed regularly to temperature changes of potential physiological significance. A laboratory study by Heaney and Eppley (198 1) showed that swimming speeds of dinoflagellates were markedly reduced at lower temperatures. 4 . Grazing Although sinking and natural death (Walsh, 1983; Billet et al., 1983) are

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locally important causes of phytoplankton mortality, leading to consumption by detritivores beneath the euphotic zone or to direct incorporation of plant material into bottom sediments, the main losses of plant cells are due to predation by planktonic herbivores in the surface layers. In considering rates of primary production, grazing not only removes part of the standing stock of phytoplankton but also indirectly promotes the continued growth of the remaining population through the release of nutritionally valuable excretory products (Corner and Davies, 1971). The relationship between primary production and grazing is therefore complex (Frost, 1980). Changes in phytoplankton biomass ( B ) with time ( t ) as a function of the rates of phytoplankton growth ( p ) and predation by grazing ( g ) can be expressed as

The various factors that determine the value of the coefficient g , including the size, type and abundance of both the phytoplankton and herbivores, are discussed by Frost (1980). Numerical modelling is an important technique for examining the range of possible dynamic states between prey and predator under natural conditions (e.g. Steele and Frost, 1977). In simple terms, grazing can be considered as the product of herbivore biomass, herbivore filtration (volume clearance) rate and phytoplankton concentration (King, 1986). However, the filtration rate is itself a function of phytoplankton concentration, and differences in the form of this relationship represent the range of feeding strategies for different herbivore species (Frost, 1980). Under stable environmental conditions, as represented by stratified, nutrient-depleted surface waters, this results in the convergence of p and g, so that the biomass of phytoplankton tends to a constant value. In other words, assuming that grazing is the major cause of phytoplankton mortality, the increase in phytoplankton biomass due to growth is balanced by losses due to grazing. By analogy with chemostat cultures at steady state (Dugdale, 1977), for which the dilution rate is equivalent to the herbivore filtration rate, this leads to the concept that grazing indirectly determines the phytoplankton growth rate (Jackson, 1980). Away from the tropical ocean gyres, seasonal changes in climatic and physical oceanographic conditions cause variations in the degree of surface mixing. These lead in turn to fluctuations in phytoplankton growth rates and to an uncoupling of growth and grazing as p and g differ. For example, in temperate regions in the spring or in recently upwelled waters, the diatom outburst is attributable to a greater increase of ,u than of g in response to stratification and favourable light conditions (Colebrook, 1986b). Subsequently, the phytoplankton biomass is reduced when nutrient depletion leads to a decrease in p while losses due to g and perhaps sinking (e.g. Billett et al., 1983) remain relatively high. However, in regions such as the subarctic North Pacific, the spring increase in phytoplankton is small and surface nutrient concen-

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trations remain high throughout the summer. This situation is thought to be due to rapid adaptations in the feeding strategy of overwintering herbivores which, as p increases, maintain comparable values of g (Frost, 1984). Changes in rates of primary production will tend to be slight, reflecting variations in p for a relatively constant plant biomass that is determined by grazing rather than climatic (light) or hydrographic (nutrients) variability. In view of the importance of grazing as a cause of phytoplankton mortality and as a means of nutrient regeneration, methods for quantifying rates of grazing under natural conditions (Roman et al., 1986) are necessary for a more complete understanding of the production dynamics of marine plankton communities. Attempts to assess directly grazing or filtration rates by mixed herbivore populations are restricted by a lack of comparative information on the feeding strategies of individual species, and by uncertainties in applying results from laboratory feeding studies to natural situations. Additional complications are the patchiness of herbivore distributions in the sea and changes in feeding behaviour (including die1 vertical migrations by the larger herbivores) in response to food availability. A new method of assessing grazing mortality based on changes in the distributions of phytoplankton pigments and degradation products in the water column (Welschmeyer and Lorenzen, 1985), has been devised to give integral measurements over periods of days to weeks. If this technique proves to be generally applicable, it could provide the first directly comparable information on grazing rates within different plankton communities. An alternative approach has been to measure nitrogen excretion by natural zooplankton populations (e.g. Dagg et al., 1980; Vidal and Whitledge, 1982). Despite unavoidable limitations of methodology and considerable variance in the results, good agreement is found between the nitrogen requirement of phytoplankton and nitrogen inputs due to the excretion of ammonium and urea and to the mixing of nitrate across the pycnocline (e.g. Harrison et al., 1985). However, no critical analysis has yet been made to show that such results are consistent with accepted values for the efficiency of nitrogen recycling by herbivores (see Corner and Davies, 1971) or with the turnover of dissolved organic nitrogen compounds (see Jackson and Williams, 1985). In other words the precise role and importance of herbivores in the various processes that lead to the regeneration of combined inorganic nitrogen within the euphotic zone, including excretion, ammonification and nitrification (Ward, 1985), remains uncertain. Recently, much attention has been given to the role of microheterotrophs (protozoa, microflagellates, bacteria) as consumers of plant carbon (for a general discussion, see Williams, 1984). Although these organisms are certainly abundant (Azam et al., 1983), much less is known about their feeding and growth than for herbivorous zooplankton which includes copepods, gastropods, and various gelatinous organisms. For temperate continental shelf waters, the available evidence still sup-

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ports the well-established concept (Steele, 1974) that the bulk of energy transfer occurs through herbivorous zooplankton (mainly copepods) feeding on phytoplankton larger than 5 pm in diameter (Ducklow et al., 1986). Under certain conditions, such as low chlorophyll water overlying a stable seasonal thermocline (Joint and Pomroy, 1983) or within blooms of the colonial flagellate Phaeocystis (Joiris et al., 1982), the utilization of plant carbon may largely be in the form of microheterotrophs feeding on autotrophic picoplankton or assimilating photosynthetic exudation products. However, in these cases, the efficiency with which plant energy is transferred to higher trophic levels is probably relatively low (i.e. much of the organic carbon will be converted to respiratory COz), the main effect of microheterotroph activity being to enhance rates of nitrogen and phosphorus remineralization (Ducklow et al., 1986).

111. METHODS FOR ESTIMATING PRIMARY PRODUCTIVITY A. NUTRIENT BUDGETS

The constant proportions of the elements carbon, nitrogen and phosphorus in growing phytoplankton cells (Redfield, 1958) allow organic production to be considered in terms of the incorporation of nitrogen or phosphorus into plant material as well as that of carbon. This approach is particularly pertinent to studies of marine productivity, as these two nutrients are thought to control phytoplankton growth in most situations (Eppley and Peterson, 1979), and deviations from the “Redfield ratios” of 106C : 16N : 1P by atoms can be indicative of nutrient-limited growth (Goldman et al., 1979; Tett et al., 1985). The development of reliable techniques for measuring dissolved inorganic and particulate inorganic forms of nitrogen and phosphorus in sea water opened the way for assessing primary productivity in terms of nutrient fluxes (Cooper, 1933). They apply specifically to rates of net production, since there are no major respiratory losses for nitrogen and phosphorus as there are for carbon. The first production estimates were based on the disappearance of nutrients during the spring bloom (see Harvey, 1950). Subsequent studies took into account vertical fluxes across the seasonal thermocline and were extended to cover the whole annual production cycle (Steele, 1956). Apart from the inherent difficulties in quantifying the effects of horizontal diffusion and advection, which are likely to be of particular importance in frontal regions, the main weaknesses of the nutrient budget approach are as follows: 1. Nutrient recycling within the euphotic zone is not taken into account, and either has to be assessed from appropriate experimental measurements or given some assumed value.

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2. It is dependent on accurate estimates (usually indirect) of vertical diffusivity. 3. For situations where the pycnocline is well within the euphotic zone (e.g. above the 1 % light level), care must be taken to specify accurately the vertical nutrient gradients which are modified by phytoplankton assimilation within the pycnocline. The first of these problems has been extensively investigated, particularly in relation to nitrogen, and statistical analyses of observational data on the relative contribution of renewal (physical mixing) and regeneration processes in supplying nutrients for phytoplankton growth have shown a significant relationship between total production and the proportion of production due to renewal or regeneration (Eppley and Peterson, 1979; Platt and Harrison, 1985). The second two are strongly site-specific, and can only be resolved through precise measurements of relevant properties within the water column (King and Devol, 1979; Eppley et d., 1979; Holligan et d.,1984b; Garside, 1985; King, 1986). With recent improvements in analytical and experimental techniques for using 15N (Dugdale and Wilkerson, 1986) and new understanding of how total production varies with the proportions of nitrogen available from renewal and regenerative processes (Harrison et al., 1987), it appears that measurements of ISNO; assimilation can be used to assess primary production. Although these methods are not yet widely in routine use, and there is still controversy about how to interpret f-ratio values (the ratio of nitrate to total nitrogen assimilation), this approach represents an important development for primary production studies, as it allows direct comparison of nitrogen and carbon assimilation rates. B. OXYGEN A N D CARBON FLUXES

Changes in dissolved oxygen provided the first direct measurements of photosynthetic production in the sea (e.g. Marshall and Orr, 1930; Cooper, 1933; Riley, 1946), and were supported by studies with cultures (Marshall and Orr, 1928; Jenkin, 1937). However, the low sensitivity of the standard Winkler technique meant that changes in oxygen could only be reliably estimated for relatively dense phytoplankton populations. Recent modifications allow measurements of dissolved oxygen in sea water with a coefficient of variation < 0.1 % on a routine basis (Bryan et al., 1976), so that even in oligotrophic ocean waters light and dark changes in oxygen levels can now be accurately determined (Williams et al., 1983). Conversion of oxygen values to carbon values depends on the photosynthetic quotient, which varies with the biochemical state of the cells, in particular with respect to the nitrogen source for growth (Williams et al., 1979; Williams, 1984). Tracer techniques based on I4CO2 largely superseded oxygen methods

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during the 1950s, as they gave greater sensitivity for production measurements (Steeman Nielsen, 1952). They have been reviewed recently by Gieskes et al. (1979) and Peterson (1980), and the various problems of interpreting data on I4CO2assimilation for marine waters are further discussed by Davies and Williams (1984) and Hitchcock (1986). As this is still the standard method for estimating rates of photosynthesis in the oceans, its main limitations must be recognized: 1. Physiological and ecological artefacts due to the enclosure of water samples in bottles cannot be fully avoided and are difficult to evaluate quantitatively. These range from direct effects on rates of carbon assimilation, to the problems of simulating fluctuations in irradiance due to mixing within the water column (Joiris and Bertels, 1985), and difficulties of interpretation introduced by secondary consumption of particulate and dissolved plant carbon during the incubation period. 2. Observed rates of carbon assimilation are likely to represent intermediate values between net and gross production, with the bias to one extreme or the other being dependent on incubation time, irradiance and rates of carbon turnover within intracellular pools (Dring and Jewson, 1982). There is still no reliable way of determining rates of phytoplankton respiration in the presence of heterotrophic organisms. 3. Compensation irradiances for different species, or for the same species under different conditions of growth (e.g. different nitrogen sources), vary by at least an order of magnitude (Hobson and Guest, 1983; Richardson ez al., 1983), so that any correction for dark respiration by natural populations can only be an approximation. 4. Uncertainties of rates of carbon exudation (Fogg, 1983) persist, owing to a combination of methodological problems and the difficulty of accounting for reassimilation by heterotrophic organisms during the experimental incubation period (Davies and Williams, 1984).

Several comparative studies of oxygen production and I4CO2assimilation have been undertaken in order to resolve some of these problems (e.g. Sakamot0 et al., 1984; Kuparinen, 1985; Shim and Kahng, 1986). For both continental shelf (Davies and Williams, 1984) and oceanic (Williams et al., 1983) waters, good agreement has been found between the two methods. Together with compatability between in situ and in vitro rates of oxygen production, this suggests that the 14C technique is not subject to any inherent source of error, although simultaneous heterotrophic activity may still introduce ambiguities into the interpretation of experimental data (Smith et al., 1984). Deviations from expected molar ratios for oxygen production to particulate carbon assimilation (the photosynthetic quotient) can be caused by differences in cell storage compounds, nitrogen sources for growth, and rates of organic carbon exudation. Such effects represent a further restriction on the use of dark oxygen changes to correct compatible measurements of photo-

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synthetic carbon fixation for phytoplankton respiration, even in the absence of heterotrophic organisms. One important and consistent observation from parallel oxygen and carbon measurements (e.g. Raine, 1983; Holligan et al., 1984b; Megard et al., 1985) is that photosynthetic quotients tend to increase at low irradiances (i.e. with depth in the water column). This result may be partly due to nitrate being a more important source of nitrogen as opposed to ammonium or other reduced compounds at the level of the pycnocline, but also probably reflects the selective utilization of photoreductant for nitrogen rather than carbon assimilation at low light levels (Megard et al., 1985). The latter effect is one explanation for anomalously high dissolved oxygen values in subsurface waters (Shulenberger and Reid, 198I ; Platt and Harrison, 1985, 1986; Craig and Hayward, 1987), and would lead to relatively low carbon to nitrogen ratios for the phytoplankton. The results from any set of oxygen production or carbon assimilation measurements must be integrated over both depth and time to give rates of production in appropriate units such as g C m-' day-'. Certain simplifications have to be made, mainly concerning the photosynthesis-light relationship, but in general it appears that these are unlikely to introduce significant errors (Mommaerts, 1982) compared to those that can affect experimental incubation procedures. Biological production may also be estimated by following in situ changes in the dissolved concentrations of oxygen and carbon dioxide in surface waters. Carbon dioxide can be determined directly as total inorganic carbon, or indirectly through appropriate measurements of pH and alkalinity (e.g. Brewer and Goldman, 1976). This way of assessing production has the advantage that many measurements can be made, so allowing better spatial coverage than with bottle incubations. Ambient carbon dioxide levels are also affected by the activity of heterotrophic organisms, and by exchanges across the air-sea interface and the pycnocline. Despite these restrictions, good agreement has been reported both between simultaneous dissolved oxygen and carbon dioxide changes (Johnson et al., 1979) and between carbon dioxide changes and I4CO2assimilation (Weichart, 1980; Codispoti et al., 1982), over periods of days to weeks. The need for improved data on spatial variability in rates of primary production, particularly in relation to physical environmental conditions, will probably lead to greater use of this approach in the future. C. BIOMASS DISTRIBUTIONS

Measurements of rates of net carbon assimilation represent a change in biomass per unit time ( A B t - I ) . Although often scaled against some measure of total biomass such as chlorophyll ,for comparative purposes, they do not incorporate or depend upon any absolute measure of biomass in equivalent

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units. Under circumstances of minimal grazing and sinking losses, as are occasionally observed in the growth phase of early spring diatom blooms (Tett et al., 1975) and of summer dinoflagellate blooms (Holligan et al., 1983a), changes in phytoplankton biomass will approximate to net primary productivity (Cushing and Vucetic, 1963; Cushing, 1983). More usually, however, such losses tend to match production (i.e. a quasi-steady-state condition is established between phytoplankton growth and mortality), and the question arises as to whether there is any relationship between the biomass or standing crop of the phytoplankton and primary productivity. This is best considered in terms of the standard equation for the specific growth rate (p)at steady state (Eppley, 1980): 1 AB p=--*B At

which can be written to a good approximation in the integrated form: 1 (B+AB) p =-In B t and gives on rearrangement: AB = B(e" - 1) Here AB is related to two variables, the biomass and the specific growth rate (Li and Goldman, 1986) of the phytoplankton population. Reliable estimates of growth rates in the sea are hard to obtain, mainly because phytoplankton carbon cannot be measured directly. A review of published data (Goldman et al., 1979) indicates that, providing that light availability is not the primary controlling factor, the annual rate of values for p is likely to be considerably less than an order of magnitude (typically 0.1 < p u > 1.0 day-') for a given region. By contrast, values of B can vary by up to two orders of magnitude or even more during the annual production cycle. On this basis some correlation between AB and B is to be expected. A relationship between these two parameters has been demonstrated for different oceanic areas, using chlorophyll as a measure of biomass (Ryther and Yentsch, 1957; Lorenzen, 1970; Eppley et al., 1985). However, there are regional differences in proportionality factors which Eppley et al. (1985) suggest are due to environmental conditions, including insolation. The main exceptions to any positive correlation between phytoplankton standing stock or biomass and the rate of primary production are likely to be when growth is limited by light, either through self shading or through deep mixing of the surface layer, and during the declining phase of blooms. With the development of techniques such as in vivo fluorometry (Lorenzen, 1965) and remote sensing of ocean colour (Gordon et al., 1983) for estimating chlorophyll over a wide range of spatial (horizontal and vertical) and temporal scales, the use of biomass as an indicator of rates of production

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could provide much new information about primary productivity in the oceans. Although the estimates may only be semi-quantitative due to difficulties of calibration, they are a source of background data on the variability of production processes in the sea which will enable more objective sampling and experimental work from ships. Furthermore, there is the possibility that ocean colour data can be directly related to productivity (Platt and Denman, 1983; Smith et al., 1983a; Platt, 1986). One major uncertainty with remote sensing techniques is variability in carbon/chlorophyll ratios for phytoplankton (Banse, 1977), which are difficult to measure since living phytoplankton generally constitutes only a minor proportion of the total particulate organic carbon in surface waters. Indirect estimates, using a variety of techniques, are generally in the range 20-100, with a mean of about 40 and values for diatoms generally lower than for dinoflagellates. D. PRIMARY PRODUCTIVITY MODELS

Recently, much effort has been put into the development of numerical models of phytoplankton growth in the sea in an attempt to simulate observed spatial and temporal changes in distributions, and to identify the parameters that control variability in biomass and/or production. These models have various aims which, in turn, reflect differences in their degree of complexity, in methods of defining the physical and chemical environmental properties, in the formulation of the growth process and in their mathematical solutions (Wroblewski, 1983). In relation to studies on primary productivity, the main emphasis has been to simulate observations at sea, and in this sense the results can only be as good as the original observations. However, attempts to match the results of real measurements and numerical models help to clarify concepts about the factors controlling phytoplankton growth in shelf seas over both short (Fasham et al., 1983a; Radach, 1983) and long (Horwood, 1982) time-scales. Of particular interest are those models that compare phytoplankton growth under contrasting physical and chemical conditions (e.g. Tett, 1981; Agoumi et al., 1985; Tett et al., 1986); they provide an objective evaluation of the effects of different environmental factors on primary productivity and indicate relative differences in total production.

IV. ENVIRONMENTAL CONDITIONS FOR PHYTOPLANKTON GROWTH IN THE NW EUROPEAN SHELF SEAS A. MIXING PROCESSES, SEASONAL STRATIFICATION

Physical properties of shelf seas relevant to biological processes, and in particular phytoplankton growth, are described by Pingree (1987b, 1980), Lee

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(1980), Simpson (1981) and Loder and Platt (1985). Here it is sufficient tc give a brief account of changes during the annual cycle that have a fundamental influence, directly or indirectly, on phytoplankton abundance. For convenience this is done with particular reference to temperature, which is the main factor determining vertical and horizontal density gradients, although salinity variations can be important, especially in the N E North Sea and Norwegian coastal waters. Thus the term thermocline (vertical temperature gradient) is used in place of pycnocline (vertical density gradient), which includes the influence of salinity on the vertical stability of the water column. Each winter the combined effects of surface cooling (heat loss to the atmosphere), surface wind mixing and bottom tidal mixing cause the water column on the shelf to become vertically homogeneous with respect to density. Any vertical gradients in temperature and salinity tend to be slight and shortlived. Horizontal gradients in these properties are also weak, although satellite images do show well-defined temperature boundaries around coasts which mark the outer extent of relatively cool, less saline, inshore water. From late winter onwards vertical stratification of the water column can develop, due mainly to river outflows of fresh water and solar warming of surface layers. Initially this change probably occurs mainly during neap tide periods. However, by April, thermohaline stratification becomes a persistent feature in regions of weak tidal mixing such as the central Celtic Sea and northern North Sea (Sager and Sammler, 1968). The horizontal extent of the seasonal thermocline is maximal by about the end of May (e.g. Pingree, 1975), but solar heating continues to strengthen the vertical density gradients until July or early August (e.g. Pingree et al., 1976), when surface-to-bottom temperature differences of 5-10°C are observed in large areas of the Celtic and North Seas. In regions of strong tidal mixing, the water column generally remains well mixed throughout the summer, although a combination of strong solar heating, low wind speeds and neap tides may allow temporary (hours to days) stratification almost anywhere. In summer, the boundaries between mixed and stratified waters tend to be characterized by horizontal temperature gradients (Pingree et af., 1975) as a result of differential heating; in stratified waters the heat input is effectively trapped in the upper 10-30 m of the water column above the thermocline, so causing relatively rapid warming (up to 2°C month-') of the surface windmixed layer and slow warming (as low as 0.1"C month-') of the bottom tidally mixed layer. By contrast, where tidal mixing prevents the formation of a thermocline, the heat input is spread through the whole water column, which may be up to 100 m deep. The rate of increase in temperature is therefore intermediate between those for surface and bottom waters in neighbouring stratified areas, so that horizontal gradients in both surface and bottom temperatures are established. These gradients become most pronounced at the surface in deep waters (see Fig. 4) and at the bottom in shallow waters, and are generally known as tidal fronts (Simpson and Hunter, 1974).

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Numerical models that predict patterns of summer stratification from information on water depth ( h ) and tidal streams (u, the mean M2 tidal current velocity) have now been well tested by comparison with observations from ships and satellite (Pingree and Griffiths, 1978). The average positions of tidal fronts (Fig. 7) are consistent with a particular value of the stratification parameter, S, which is defined as S = log,,, (h/CdU3)(Cd is a dimensionless drag coefficient), and generally show only small deviations in position in response to wind effects or spring-neap tidal cycles (Simpson and Bowers, 1979). However, as with all types of frontal boundary, they are subject to various forms of instability (Pingree, 1978a) which, together with any advective effects, can lead to gross movements over scales of tens of kilometres (e.g. Pingree et a/., 1977a). Such effects are important in determining rates of cross-frontal exchange of water properties, including inorganic nutrients and planktonic organisms. In a similar manner, the seasonal thermocline, which represents the subsurface extension of surface fronts (see Fig. 4), is affected by physical mixing processes that determine vertical exchange or diffusion within the water column (Pingree and Pennycuick. 1975). The dissipation of internal wave energy (Pingree and Mardell, 1985) is now thought to make an important contribution to this process, as well as the effects of winds and tides. By autumn surface cooling and increased wind mixing lead to the erosion of tidal fronts and the seasonal thermocline. There is a general weakening of the density (thermal) gradients and some gross displacement of the boundaries; surface fronts retreat as the region of stratification becomes smaller (Pingree, 1975), and the thermocline deepens in response to increased mixing at the surface (Pingree et a/., 1976). However, the timing and progress of such events are irregular, so that the effects on biological properties may be quite different from one year to the next. Against this background of seasonal change in the physical environment, it is necessary also to distinguish chemical and biological factors that affect phytoplankton distributions in order to gain some overall understanding of primary production processes in the shelf seas of NW Europe. From a general analysis of plankton patchiness, Mackas et al. (1985) concluded that physical effects are dominant only at small scales. Examples are Langmuir circulation patterns in which phytoplankton cells showing directional motility or buoyancy are accumulated (Le Fevre, 1986), and boundary zones such as the seasonal thermocline where rates of turbulent diffusion may be low enough to allow aggregations of cells to persist (Pingree, et al., 1975). By contrast, at larger scales, phytoplankton distributions are largely determined by a combination of the availability of resources (i.e. light and nutrients, which in turn are controlled by physical conditions), by the growth responses of individual species, and by the activities of herbivores (see Taylor et a/., 1986).

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Fig. 7. Distribution of mixed, frontal and stratified waters for the NW European shelf in summer, based on the numerical model of Pingree and Griffiths (1 978) for the stratificationparameter, S (see text). B. LIGHT AVAILABILITY

The seasonal and daily ranges of sea surface irradiance can be inferred from meteorological data. With the latitude and climatic conditions of the NW European shelf, daily irradiance values vary by about one order of magnitude between mean winter and summer conditions, and between overcast and clear days at any one time of the year (e.g. Mommaerts, 1973). On an annual basis, total irradiance decreases from south to north by approximately 30% between 50"Nand 60"N. Except for surface albedo losses, which are usually 10% (Payne, 1972), it

-

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22 1

Fig. 8. Atmospherically corrected Coastal Zone Color Scanner image (Channel 2, 510530 nm) for the southern North Sea on 5 March 1982 (courtesy of S. Groom). Light areas indicate reflective waters with a high suspended sediment load, and dark areas relatively clear waters which are least reflective (i.e. darkest) where there is significant absorption by plant pigments. CI, clouds.

is the properties of the water that determine the proportion of light available for photosynthesis. Over most of the continental shelf surface, salinities remain > 34K, so that variations in light absorption due to the water itself, including dissolved substances, are unlikely to be great (Hajerslev, 1983, 1982). Thus the main factor affecting the light environment for photosynthetic organisms, apart from self-shading which is a function of chlorophyll concentration, is scattering by suspended particulate matter (Topliss et al., 19808 1 ; Topliss, 1982; Hajerslev, 1982). The extremely heterogeneous distribution of surface turbidity is well shown by satellite ocean colour images (Fig. 8; Mitchelson et al., 1986), from which maps of the attentuation coefficient can be derived (Viollier and Sturm, 1984). Due to the difficulty of making appropriate continuous in situ measurements, there is relatively little published data on attenuation coefficients for the NW European shelf seas as a whole. Surveys have been made with the Secchi disc (e.g. Tijssen, 1968; Holligan et al., 1978), and with instruments that measure turbidity or beam transmission (Lee and Folkard, 1969;

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Pingree et al., 1986). Together with irradiance profiles for discrete stations which are often made in conjunction with primary production measurements, these suggest that KO is generally in the range 0.084.60 m-', with values >0.20 m-' confined to well-mixed, turbid coastal waters and to exceptional phytoplankton blooms (e.g. Holligan et al., 1983a). In the absence of significant light absorption by chlorophyll, higher KOvalues are consistently observed close to the shore, but gradients normal to the coastline are very variable (Pingree et al., 1986) and are often characterized by large variations at boundaries between different water masses (Brylinski er al., 1984). Within offshore coccolithophore populations, rather unusual light conditions prevail due to a combination of low absorption by relatively low chlorophyll concentrations and strong scattering (high reflectance) by coccoliths (Holligan et al., 1983b). The range in attenuation coefficients sets broad limits on light availability for photosynthesis, assuming that the depth of the surface mixed layer (i.e. the degree to which phytoplankton cells are held within the euphotic zone) is known. If other factors, such as nutrients and grazing, did not limit primary production, the combined effects of light attenuation and depth of mixing would effectively determine production rates. This premise has led to the use of the parameter kh (the light attenuation coefficient, k , scaled by the water depth, h) for defining the light environment of natural phytoplankton populations in shelf waters (Pingree et al., 1978b; Bowman et al., 1981). Together with information about surface irradiance, such an approach allows an objective comparison of light regimes and the ability to predict for any given region the start and end of the phytoplankton growth season (see Figs 8 and 21 in Pingree (1978b)). For stratified waters, h is effectively given as the mixed layer depth, so that the change in light availability resulting from the onset or breakdown of stratification can also be assessed. On the NW European shelf, phytoplankton growth can be restricted by light throughout the year, both in turbid estuaries such as the Bristol Channel, for which a 20-fold range in annual productivity values has been described (Joint and Pomroy, 1981), and in deep, relatively clear waters where strong tidal mixing prevents the formation of a seasonal thermocline (Pingree et al., 1978; Martin-JCzequel, 1983). By contrast, in some regions the water is sufficiently clear and shallow (i.e. low kh value) that some net production may occur even in the winter-see Postma (l978), who infers this to be the case for parts of the southern North Sea where winter levels of inorganic nutrients remain relatively low. In most deeper waters ( > 6 0 m), which became stratified in the summer, the development and breakdown of the seasonal thermocline is probably the main factor in determining the length of the growth season (e.g. Pingree et al., 1976), but in shallow waters the combination of seasonal changes in irradiance and low kh values is likely to be more critical. The seasonal thermocline and associated subsurface chlorophyll maxi-

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mum represents a special type of light environment. Due to light attentuation within the wind-mixed layer, the plant cells are exposed to a restricted range of irradiance and will, in general, show positive net photosynthesis only in relatively clear weather (Holligan et al., 1984b). This has important implications both for estimates of water column productivity and for understanding the potential effects of light on nutrient fluxes across the thermocline (Taylor et ul., 1986). With the recent advances in understanding how tides largely determine the development of the seasonal thermocline and the positions of frontal boundaries between stratified and mixed water masses, it appears that predictions of the effects of light on phytoplankton growth are limited mainly by a lack of information about variations in values for K O .A more detailed analysis of satellite imagery for the visible wave band (Hrajerslev, 1982; Viollier and Sturm, 1984) will be one approach to resolving the problem. C. NUTRIENT AVAILABILITY

As already indicated, nutrient availability acts as a secondary control on primary production in temperate shelf seas once there is sufficient light for the plant cells to grow. To a first approximation, total annual primary production is likely to be proportional to the quantity of new nutrients (i.e. derived from deep water and/or winter regeneration in surface layers) assimilated by the phytoplankton (Eppley and Peterson, 1979). On the NW European shelf, maximum surface concentrations of inorganic nutrients are usually observed in late winter before uptake by phytoplankton in the spring starts to exceed rates of regeneration from dissolved and particulate organic materials in the water column and sediments. Levels of nitrate nitrogen and phosphate phosphorus reach 6-12 ,UMand 0.4-0.9 ,UMrespectively (e.g. Johnston and Jones, 1965; Pingree et al., 1976; Postma, 1978; Foster, 1984; Brockmann and Wegner, 1985), but are higher in estuarine and some inshore waters. In terms of the annual turnover of dissolved nitrogen and phosphorus, net losses from shelf waters in the form of fluxes of particulate matter to the sediments and of dissolved organic matter to deep ocean water are mainly balanced by oceanic inputs, with Atlantic water probably accounting for about 80% of the total nutrient supply for the shelf ecosystem (e.g. Gerlach, 1981). Most of the remainder comes from fresh-water inputs (precipitation, land drainage), but only locally within semi-enclosed regions distant from the shelf break, such as the southern North Sea, are these the dominant nutrient sources (Postma, 1978, 1985). In the spring and summer the inorganic nutrients are assimilated by the phytoplankton, with surface concentrations being reduced typically to < 0.5 PM nitrate nitrogen and CO.1 ,UM phosphate phosphorus. In mid-summer, appreciably higher values are restricted to mixed coastal and estuarine waters

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characterized by high kh values. The nitrate to phosphate ratio tends to decrease with depletion (e.g. Pingree et al., 1977b), suggesting that nitrate is in shorter supply, possibly as a result of less rapid regeneration. Exceptions to this are in parts of the southern North Sea, where low phosphate appears to limit phytoplankton growth (Postma, 1978; Veldhuis and Admiraal, 1989), and within diatom blooms, where silica may restrict diatom growth. Surface concentrations of nitrate above a stable thermocline can fall to G0.02 PM with very low standing stocks of phytoplankton (GO.1 mg chlorophyll a m-3). The summer reduction of nitrate and phosphate in surface stratified waters is largely balanced by increases in dissolved organic nitrogen and phosphorus (Butler et al., 1979). Only within dense phytoplankton blooms do concentrations of particulate nitrogen and phosphorus ever exceed those of dissolved forms. In regions of weak tidal mixing, levels of inorganic nutrients below the thermocline increase during the summer due to continued regeneration in deep water and the bottom sediments (e.g. Pingree et al., 1976; Morin et al., 1985). However, where tidal mixing is stronger and the thermocline less well developed, the upward fluxes of nitrate and phosphate balance or exceed rates of bottom regeneration. This effect promotes more efficient utilization of the nutrient stock within the water column, and provides an explanation for higher standing stocks of plankton in weakly stratified and frontal areas (Holligan, 1981); it may be further reinforced by spring-neap cycles of tidal mixing (Pingree et al., 1977a) and by the advection of nutrient-rich bottom water (Morin et al., 1985). During the summer, both in mixed and stratified waters, the available nitrate (and inorganic phosphate) for phytoplankton growth is supplemented by regeneration processes. More is known about the recycling of nitrogen, as standard methods have been developed for measuring the products of heterotrophic activity, such as ammonium, urea and amino acids, in sea water. However, no really consistent picture has yet emerged of the distributions and fluxes of these compounds. With the prevailing low concentrations in offshore waters, samples must be analysed immediately for reliable determinations and there are considerable experimental difficulties in estimating rates of turnover. There is evidence that ammonium (Foster et al., 1985; Q u S guiner et al., 1986), urea (Turley, 1986) and amino acids (Poulet et al., 1984; Williams and Poulet, 1986; Flynn and Butler, 1986) are all important sources of nitrogen for natural phytoplankton populations, and the addition of such compounds is known to stimulate photosynthetic rates (Davies and Sleep, 1981). On the other hand, attempts to estimate nitrogen requirements, together with observations on zooplankton excretion (Holligan et al., 1984b; Harris and Malej, 1986), indicate that most of the regenerated nitrogen is supplied as ammonium. In autumn, increased mixing across the thermocline, due to surface cooling and wind, enhances the supply of nutrients to the surface mixed layer. But

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the balance between this process and the maintenance of an adequate light regime (a combination of surface irradiance and stability) does not always allow the development of a well-defined autumn bloom. As a result, the timing and extent of increases in phytoplankton biomass at this time of year are irregular (e.g. Pingree et al., 1976). Although no detailed analysis of regional variations in nutrient distributions on the NW European shelf has been carried out, it is apparent that mixed, frontal and stratified waters are quite distinct in this respect (e.g. Savidge and Lennon, 1987). The underlying causes include variations in the depth of the mixed layer (or water column for unstratified waters), which define the initial nutrient input, and the relative importance of light and nutrients in controlling growth, as well as differences in mixing rates across the seasonal thermocline (see Holligan et af., 1984b), and the effects of advection, eutrophication and short-term regeneration (i.e. excluding winter regeneration) which determine nutrient supply during the summer period. Examples of seasonal changes are provided by Baeyens et af. (1 984) for inorganic nitrogen in the southern North Sea, and by Butler et al. (1979) and Wafar et al. (1983) for nutrients in stratified and mixed waters of the western English Channel. Regenerated nutrients tend to be relatively more important in surface stratified waters due to restricted renewal across the seasonal thermocline, although rates of regeneration can be higher in eutrophic inshore waters.

D. GRAZING

Herbivorous zooplankton, apart from acting as a source of regenerated nutrients, directly affect primary productivity whenever the grazing rate is significantly different from the phytoplankton growth rate. Cushing ( I 983) discusses the evidence for the control of plant production by herbivores based on the observation that the spring maximum in plant biomass is reached before the main decline in nutrient levels. There is also evidence to suggest that grazing lags behind primary production allowing a significant proportion of the phytoplankton to sink through the developing thermocline (Davies and Payne, 1984) and be consumed by benthic organisms (Fransz and Gieskes, 1984). The control of phytoplankton biomass by herbivory depends on an increase in the reproductive rate of the plant cells being matched by an increase in grazing rates due to reproductive strategies (e.g. Williams and Conway, 1984) or aggregation (Fransz and Diel, 1985) of the herbivores. However, once the water column is stratified the inorganic nutrients are depleted over a period of 1-4 weeks, depending on the stability of the thermocline, to uniformly low levels (e.g. Pingree er al., 1977b). This condition indicates that nutrient availability rather than grazing is the overall factor limiting primary

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production during the spring months. Subsequently a quasi-steady-state condition is reached, with nutrient input (renewal across the thermocline plus regeneration), phytoplankton growth and herbivory in balance with one another. The grazers are the dominant cause of algal mortality and provide a large proportion of the regenerated nutrients. Thus, the behaviour, feeding, growth and excretion of herbivores such as copepods (e.g. Williams and Conway, 1984; Daro, 1985; Die1 and Klein Breteler, 1986; Harris and Malej, 1986) influence both the growth (nutrient assimilation) and survival of phytoplankton cells. For the shelf waters of NW Europe the copepods are generally considered the dominant herbivores, with other groups such as protozoa (e.g. Admiraal and Venekamp, 1986) locally important. However, in surface stratified waters it appears from biomass distributions (Holligan et al., 1984a; Fogg rf al., 1985), from the abundance of small ( < 5 pm diameter) autotrophic cells which are not captured efficiently by copepods (Joint and Williams, 1985), and from grazing experiments (Burkill et al., 1987), that much of the grazing is by microheterotrophic organisms, including non-photosynthetic dinoflagellates (Jacobson and Anderson, 1986). It is still difficult to take proper account of these organisms in constructing carbon budgets for marine ecosystems due to the lack of information on rates of feeding and excretion within natural populations. This problem is well illustrated by attempts to define the role of bacteria. Although bacterial activity is found to be coupled to primary production and is important in remineralization processes (Lancelot, 1924; Lancelot and Billen, 1984; Lochte and Turley, 1985), there is much uncertainty about how much of the carbon flow to higher trophic levels is through bacteria. Observational data (Holligan et al., 1984b; Joint and Williams, 1985) indicate that microheterotrophic organisms are relatively unimportant for the food chain except through their contribution to remineralization, whereas theoretical considerations have led to the opposite viewpoint (Newell and Linley, 1984). Persistent blooms of dinoflagellates, in which increases in cell density over a period of several weeks are associated with relatively low abundances of herbivores (Lindahl and Heinroth, 1983; Holligan et al., 1984a), represent a special case. The combination of reduced grazing rates, perhaps due to some inhibitory effect and assimilation of nutrients from subthermocline water (Holligan et al., 1984b), lead to high phytoplankton biomasses, with the standing stocks of particulate carbon and nitrogen per unit area representing a relatively large proportion of annual primary production values.

E. ANNUAL PRODUCTION CYCLE

Various attempts have been made to summarize the observed changes in phytoplankton abundance and species composition in temperate marine ecosys-

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tems with respect to environmental conditions. A generalized scheme of events is shown in Fig. 9, based on the analysis of Bowman et al. (1981). Differences in light and nutrient availability, which are determined primarily by the timing of thermocline establishment and breakdown, cause a divergence in terms of phytoplankton growth rates and species succession. This effect is made clearly apparent by comparing seasonally stratified waters with those that remain well mixed throughout the year (e.g. Maddock et af., 1981). In regions adjacent to frontal boundaries where stratification develops late and is eroded early, the growth season may only be half as long as in areas of persistent seasonal stratification (see Pingree, 1975). In general, in the former situation there is a tendency for the summer flagellate communities to last a relatively short time and for the autumn diatom bloom to be more pronounced. In mixed water regions, depending on the depth and turbidity of the water column, kh values may be sufficiently large to allow only a weak diatom bloom in mid-summer, or, at the other extreme, low enough for the depletion of inorganic nutrients and the replacement of diatoms by other phytoplankton types. Significant year-to-year and longer term (Colebrook and Taylor, 1984; Radach, 1984) differences in phytoplankton distributions are also likely to occur in response to climatic variability which, through the effects of wind and solar radiation, determines the stability and light environment of the surface layer. The various seasonal patterns for phytoplankton abundance in the shelf waters of NW Europe, as illustrated in an idealized form in Fig. 10, reflect differences in kh values and in timing of thermocline formation and breakdown. There is considerable evidence both from field observations and from modelling work that these are representative of the range of shelf water environments.The main problem is to evaluate such distributional patterns in terms of net productivity. Statistical analyses (Jordan and Joint, 1984; Platt, 1986) suggest that, for a relatively restricted area where variations in annual insolation are small, biomass and productivity are correlated. However, regional and temporal differences in the vertical distribution of light and chlorophyll, in P-Z relationships, in carbon-nitrogen and carbon+hlorophyll ratios and in other properties determined by the species composition and age of populations indicate that such a simple relationship is unlikely. For example, within frontal dinoflagellate blooms, it appears that both net productivity per unit area and growth rate of the population decline as standing crop increases and self-shading leads to light limitation (Holligan et af., 1984b3.

V. EVALUATION OF PRIMARY PRODUCTIVITY ESTIMATES A. GENERAL CONSIDERATIONS

The main objective of marine primary productivity studies is to estimate net

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S D

3

2

1 I

I

I

10

1

0.1

I

kh 2-

4-

void

10 Fig. 9. Diagrammatic representation of the seasonal succession of phytoplankton in relation to changes in water column illumination, kh, and vertical stability, S. Although the sequence of events in space and time cannot be fully defined in terms of two parameters, realistic values for kh and S are indicated (see text for definition of terms). Note that kh is plotted on a logarithmic scale. An alternative measure of surface layer stability is shown by values for D,the vertical diffusivity across the pycnocline (cm2s-l). Modified from Bowman et al. (1981).

photosynthetic carbon fixation for the whole, or some defined part, of the annual cycle. Ideally, information on the production of dissolved as well as particulate organic carbon should be included. Furthermore, with respect to food chain dynamics, the efficiency with which different forms of plant carbon (i.e. large cells, small cells, dissolved material) is also of interest, although such details lie beyond the scope of this account. The nutrient budget approach to estimating primary productivity in shelf waters is based on standard, well-accepted ratios for carbon, nitrogen and phosphorus in plant material, on precise measurements of changes in nutrient concentrations in the water column, and on some objective assessment of nutrient recycling (e.g. Owens et al., 1986). Uncertainties in parameters such

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Mixed

Shallow

Mixed

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2 1

I

F

Fig. 10. Predicted annual changes in net primary productivity for different water types on the NW European shelf. S, spring outburst; DB, dinoflagellate bloom; A, autumn bloom. The vertical scale, although arbitrary, does indicate relative changes in rates of phytoplankton production.

as vertical diffusivity and vertical nutrient gradients, which are critical for more precise estimates of nutrient fluxes (e.g. Steele, 1956), can be corrected as improved observational data become available. Also, the significance of horizontal gradients in nutrient concentrations such as occur across frontal boundaries can be semi-quantitatively assessed (Loder and Platt, 1985). Essentially similar results are obtained from budgets for phosphorus or nitrogen, although those for nitrogen have received greater attention in recent years as regeneration processes have become better understood. Few detailed nutrient budgets have been prepared for the shelf waters of NW Europe. However, they are of particular importance as they consider phytoplankton growth over extended time periods (e.g. an annual cycle), and also take into account spatial variations in the basic physical and chemical

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properties of the water column. Also they are fully compatible with ecological models in which nutrients and light are the forcing functions (Tett et al., 1986; Taylor et al., 1986). By contrast, measurements of photosynthetic carbon fixation using the I4C method, which represent the main source of information on primary productivity, are difficult to interpret with respect both to the distinction between net and gross production and to the problems of extrapolation from the results of short-term experiments (often < 6-h incubation periods) to daily or longer-term production rates. Furthermore, 14C02 fixation experiments effectively provide only point values which, for practical reasons, cannot be obtained with sufficient frequency to allow a realistic appraisal of temporal and spatial variability in the primary productivity of heterogeneous physical environments such as the NW European shelf region. For this reason, particular care must be taken to check that experimental incubations are carried out under a representative range of light conditions, and that subsurface features such as chlorophyll maxima are adequately sampled. As emphasized by Platt and Harrison (1985), as much attention should be given to variances as to means in considering the overall dynamics of the growth of natural phytoplankton populations. The main value of 14C02uptake experiments has been in examining particular features of the growth characteristics of phytoplankton, such as the effects of light and nutrient levels on photosynthetic rates, the exudation (excretion) of organic carbon, and the relationship between biomass and potential productivity. Net productivity values based on the I4C method alone depend on some explicit correction for or assumption about plant respiration. If the activity of heterotrophic organisms is relatively slight, 24-h incubations with I4CO2may provide a direct measure of net photosynthesis or, alternatively, corrections for respiration can be made by comparing I4CO2 uptake rates in the light with the results of parallel measurements of light and dark changes in oxygen, of nutrient uptake and of pH shifts. However, in reviewing the published data, it is apparent that such supplementary information is generally unavailable. ,Most 14C02productivity estimates deal only with particulate organic carbon. Mainly for methodological reasons, there are still relatively few reliable measurements of exudation that can be considered relevant to natural situations. On the whole they indicate exudation rates of about 10% of total carbon fixation, although it is difficult to take into account possible reassimilation of organic matter by the plant cells, as shown recently for Phaeocystis colonies (Veldhuis and Admiraal, 1989, or by heterotrophs. The ecological significance of phytoplankton exudation therefore remains uncertain. Regardless of method, any overall assessment of primary productivity in NW European shelf waters must also deal with a major inconsistency in the interpretation of observational data; certain estimates of plant production

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(e.g. Steele, 1956) continue to be accepted as representative of the whole shelf ecosystem, whereas advances in understanding the effects of physical mixing processes on the environmental conditions for phytoplankton growth (Pingree, 1980) indicate that regional variations in annual productivity are considerable. Although there is increasing evidence from comparative studies at different sites for such regional variability (e.g. Gieskes and Kraay, 1984), objective methods for defining or predicting the range of annual production values have yet to be established. B. MIXED WATERS

Strong tides maintain well-mixed water conditions during the summer months in much of the Irish Sea, the southern North Sea, and the eastern English Channel extending westwards along the coast of NW France (Fig. 7). In these regions the combined effects of variations in depth and turbidity (i.e. kh) lead to a wide range of primary productivity values; for example, 20-fold differences in annual (gross) rates have been reported for the Bristol Channel (Joint and Pomroy, 1981). However, rates of net production are difficult to establish, partly because phytoplankton respiratory losses can be a high proportion of gross photosynthetic fixation, leading to large potential errors in estimates of the small differences between the two, and partly because the rates of nutrient inputs from rivers and from regeneration processes in the water column and sediments are hard to assess. A further problem is that changes in irradiance experienced by the plant cells as a result of vertical motion are not easy to simulate in a productivity experiment, leading to possible errors in the parameterization of the P-I curve, except when the timescale of mixing is too short to allow photoadaptive responses (Uncles and Joint, 1983). The most detailed investigations of phytoplankton growth in mixed waters have been undertaken off the Belgian coast. A recent summary (Joiris et al., 1982) gives a value of 320 g C m-2 yr-l, based on measurements by the 14C02 method, for total net primary production of which 60% is in a particulate form. However, it is not clear how corrections were made for phytoplankton respiration. A major discrepancy between carbon and oxygen fluxes is interpreted as evidence for rates of gross primary production up to 2000 g C m-2 yr-I, a much higher value than has been reported for other areas. Other I4C estimates of particulate primary production are > 300 g C m-2 yr-' in coastal waters off NW France (Wafar et al., 1983) 200-250 g C m-2 yr-l in the Southern Bight (see Fransz and Gieskes, 1984), about 140 g C m-* yr-l in mixed waters of the western English Channel (Boalch et al., 1978), and 7-165 g C m-2 yr-' in the Bristol Channel (Joint and Pomroy, 1981). These data cannot be compared directly, owing to different sampling and experimental procedures, but there is evidence from separate areas for a positive correlation between chlorophyll concentration and the rate of primary

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productivity. The effects of turbidity and water depth on productivity are clearly demonstrated (e.g. Joint and Pomroy, 1981), and there is general agreement between various estimates of daily and seasonal productivity for the southern North Sea (Gieskes and Kraay, 1975,1977; Lancelot and Billen, 1984; Veldhuis et al., 1986b), with the highest values for the less turbid offshore waters. Rates of exudation are very variable, but are commonly 10% of total production even in the presence of mucilaginous colonies of Phaeocystis (Joint and Pomroy, 1981; Veldhuis et af., 1986a). Hydrographic data for the Southern North Sea (Brockmann and Wegner, 1985) and eastern English Channel (Holligan ef af., 1978) show that the spring phytoplankton bloom may begin locally as early as February, and a winter nutrient minimum over the Dogger Bank is indicative of net growth of the phytoplankton throughout the winter (Postma, 1978). However, both for these regions and for the Irish Sea, no annual estimates of primary production appear to be available even though seasonal studies of I4CO2fixation have been undertaken (Gros and Ryckaert, 1983). A model for phytoplankton growth at a mixed water station in the central English Channel (Agoumi et al., 1985) gives a gross productivity value of 35 g C m-z yr-I, which seems unrealistically low. Brander and Dickson (1984) have suggested that low levels of fish production in the Irish Sea may be related to a short phytoplankton growth season and low annual productivity. A mean irradiance level of about 0.03 cal cm-' day-' is required to allow positive net production in a mixed water column (see Gieskes and Kraay, 1975; Pingree et al., 1976), and increases in phytoplankton biomass occur once this value is exceeded. However, changes in species composition (Maddock et af.,1981) are observed when no net production is predicted, perhaps as a result of temporary relaxation in vertical mixing at times of sunshine, low wind speeds and neap tides. Exceptionally early blooms can also develop (Boalch et af., 1978; Reid et af., 1983) in association with strong river outflows, and these may be an important source of variability in annual productivity. It is important to note that gross production will always be measurable in winter (Fransz and Gieskes, 1984) as long as there is phytoplankton in the water, but will largely be dissimilated by respiration. The mixed water regions of the NW European shelf are affected by nutrient inputs from the major rivers, and are therefore likely to show changes in productivity as a result of hypernutrification. There is little direct evidence for this hypothesis . However, Postma (1978) suggests that there may have been a 20-40% increase in primary production in the southern North Sea over the last few decades, and that the widespread Phaeocystis blooms in the spring may be the result of higher inputs of nitrogen and phosphorus as opposed to silicon, a lack of which now restricts diatom growth. The increase in abundance of Phaeocystis at the entrance to the Wadden Sea has been documented by Cadee and Hegeman (1986), and nutrient models for Dutch coastal waters indicate a doubling of primary production between 1930 and

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1980 (Fransz and Verhagen, 1985). Wafar et af. (1983) report substantial increases in annual mean and daily maximum production values in Morlaix Bay (NW France) between 1966 and 1986 which they ascribe to increases in available nitrogen.

C. STRATIFIED WATERS

Over most of the NW European shelf the water column is stratified during the summer months (Fig. 7), with the thermocline becoming established in April and May and persisting in areas of weak tidal mixing until early winter (e.g. Pingree, 1975). The first detailed estimates of net primary production were made by Steele (1956) for the northern North Sea from an analysis of 3 years’ data on phosphate distributions. The annual values ranged between 54 and 127 g C m - 2 yr-l, being lowest in offshore areas where vertical mixing is weak in the summer and highest in inshore waters off NE Scotland. One uncertainty in the calculations concerned the rate of phosphate regeneration in the surface layer, and the assumption that this is not zero but the same as in the bottom layer increased the productivity estimates by 25-33%. Also, considerable differences between the years were apparent, due mainly to variations in vertical mixing in the summer and autumn. Almost all subsequent models of the North Sea food chain have used an average net primary production rate of 100 g C m-? yr-I based on Steele’s work (e.g. Jones, 1984). Another phosphate-based production budget for Station E l in the western English Channel was described by Pingree and Pennycuick (1975). In this case the temperature and nutrient data were the averages of many years observations. For a shallower water column than the northern North Sea and lower winter maximum phosphate levels, the annual production was again calculated to be about 100 g C m-* yr-’, with about one-quarter attributable to the seasonal reduction in ambient dissolved inorganic phosphate and the remainder to recycling processes. Regeneration rates were estimated for the bottom mixed layer and assumed to be uniform through the whole water column. In both these studies water bottle sampling at 10-m intervals did not allow the gradients in phosphate across the thermocline to be accurately defined. Using a continuous pump sampling technique, Holligan et af. (1984b) showed that vertical distributions of nitrate are strongly modified by uptake in the subsurface chlorophyll maximum, and that under extreme conditions within a dinoflagellate bloom the change between surface and bottom layers is confined to the very base of the thermocline. For a given mixing rate, the upward flux of nutrient will be proportional to the nutrient gradient, which may vary by more than an order of magnitude (Holligan et al., 1984b). Thus the earlier estimates of net primary production rates in stratified waters based

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on vertical phosphate fluxes must be considered as minimal values, especially as a faster removal of phosphate from bottom water associated with a steeper vertical gradient in concentration would also imply more rapid rate of regeneration. Steele (1957a,b) showed that dissolved oxygen measurements and the results of a few I4Cexperiments supported the phosphate productivity estimates. Since then the only intensive study of primary production in the northern North Sea has been the FLEX study in the spring of 1976. From a comparison of methods based on pH changes, nutrient uptake and I4C uptake, net carbon fixation between the end of April and beginning of June was about 30 g C m-2 (see Weichart, 1980). This approach has yet to be applied to the full annual cycle. For other areas of stratified water, annual production values based on the 14Cmethod are -250 g C m-2 yr-' in the central North Sea (Gieskes and Kraay, 1980), 180 g C m-2 yr-l in the western English Channel (Russell et af., 1971; Boalch et af., 1978), and 100 g C m-2 yr-I in the Celtic Sea (Joint et al., 1986) and in Norwegian fjords (Erga and Heimdal, 1984; Eilertson and Tasen, 1984). However, these figures are not really compatible, being based on different ways of distinguishing net and gross primary production and on different sampling strategies. Furthermore, for a single location, Station E 1 off Plymouth, a measure of the uncertainty is given by the range of published values (all g C m-'yr-'): 180 from l4Cexperiments (Russell et al., 1971), 100 from a phosphate budget (Pingree and Pennycuick, 1975), and 70 from a model of phytoplankton growth (Agoumi et al., 1985). It seems likely that the average net annual primary productivity at this station is between the first two values. A model for a similar site in the west central North Sea also gave an anomalously low net production value of 37 g C m-2 yr-' (Horwood, 1982), although this figure was considered reasonable in terms of relatively low winter nutrient concentrations and a shallow mixed layer in summer. Other I4C data for phytoplankton productivity in stratified waters relate mainly to daily rates at particular stations. Most measurements are for midsummer, when the phytoplankton biomass is relatively low and growth is supported mainly by nutrient regeneration. Daily fluctuations in production rates are considerable (e.g. Joint and Pomroy, 1983), reflecting variations in irradiance and perhaps in the species composition and physiological properties of the phytoplankton (Joint and Pomroy, 1986), but mean values may be a reasonable approximation of net productivity under conditions of relatively small respiratory losses. Rates of about 0.5 g C m-2 day-' appear to be typical (Joint and Pomroy, 1983; Holligan et af., 1984b; Joint et al., 1986), but rates tend to be higher close to frontal zones (Jordan and Joint, 1984; Gieskes and Kraay, 1984) and lower in the most strongly stratified water (Steele, 1957a). The seasonal thermocline persists for several months over a large propor-

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tion of the NW European shelf (Fig. 7). For this reason, low-nutrient stratified waters, although exhibiting relatively low daily rates of production, make a substantial contribution to total annual productivity. Some assessment of range and va,riability in production rates in such waters is therefore required. At two stations in the western English Channel, Holligan et al. (1984b) estimated upward fluxes of nitrate to be 5.74 and 3.22 pg nitrate nitrogen cm-2 day-'. A similar calculation for the region of strong stratification of the north central Celtic Sea, based on the hydrographic data of Pingree et al. (1976), gives < 0.5 pg nitrate nitrogen cm-* day-' assuming that a subsurface chlorophyll maximum is present within the thermocline. Although this order of magnitude difference may be partially offset by more efficient recycling of nutrients at the more oligotrophic station, it does suggest large regional variations in summer production rates even in waters unaffected by frontal blooms (see following section). A similar conclusion is drawn from observations of pH distributions in the German Bight (Weichart, 1985) which indicate primary production values 2-3 times those of the open North Sea. As pointed out by Steele (1956), relatively little is known about primary production in the autumn. Seasonal studies of biomass (Reid, 1978; Holligan and Harbour, 1977) and productivity (Boalch et af., 1978) show increases at this time of year, but the autumn outburst remains a somewhat enigmatic event in terms of its overall contribution to annual productivity, especially as much of the organic carbon may be subsequently lost through phytoplankton respiration as the water column becomes well mixed. On the other hand, in regions such as the central North Sea it may be as important as the spring bloom (Cushing, 1983).

D. FRONTAL REGIONS

Rates of primary productivity are least well documented for frontal regions between well-mixed and seasonally stratified waters (Fig. 7), partly because their biological significance has only recently been recognized, and partly because the problems of sampling within a complex physical environment are considerable. Furthermore, although tidal fronts often show relatively high standing stocks of phytoplankton, there are strongly divergent opinions as to what these signify in terms of biological production processes. The physical properties of frontal boundaries are variable with respect to cross-frontal gradients in density, spring-to-neap differences in tidal streams, water depth, along-frontal advective flow, cross-frontal instabilities (i.e. eddies) and exchange etc. Biological properties also vary, both spatially and temporally, within any frontal region and between different fronts, as is well illustrated by surveys (Pingree et al., 1978; Savidge and Foster, 1978) and seasonal studies (Holligan, 1981; Richardson et al., 1985) of phytoplankton

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distributions. During the summer months at least three patterns can be recognized (see also Fig. 10): 1. Deep ( > 60 m) water fronts where nutrients remain relatively high in both mixed and subthermocline waters, and maximum chlorophyll concentrations are at the front boundary and extend into the shallow thermocline (Pingree et al., 1982). 2. Shallow ( < 60 m) water fronts where the main horizontal temeprature gradients are in the bottom water, nutrient levels are generally low. and chlorophyll maxima can be displaced to the stratified side of the frontal boundary (Creutzberg, 1985). 3. Localized fronts for which the length scale of the boundary is relatively small compared to the rate of along-frontal advection so that any increase in chlorophyll due to growth is masked by dispersion within surrounding waters (Jones et al., 1984). Intermediate situations are also found, especially in shallow waters where the balance between light and nutrient effects on phytoplankton growth is strongly influenced by varying weather conditions (sunlight, wind mixing). There is no time series of primary productivity measurements for a single frontal region, although comparative observations on frontal, stratified and mixed waters have been made (Fogg et al., 1985). For conditions where the bloom dinoflagellate, Gyrodinium aureolum, has been absent, higher rates of photosynthetic carbon fixation have been found close to the front compared to well-stratified waters (Richardson, 1985; Richardson et al., 1986; Videau, 1987), with maximum values up to 1.8 C m-2 day-'. In the latter two studies, no significant differences in rates of primary productivity were found between frontal and well-mixed stations, but the possibility of relatively high losses of carbon in the mixed waters due to dark respiration were not considered (see Holligan et a[., 1984b). Most other production measurements in frontal regions relate to blooms of G . aureolum (see Partensky and Sournia, 1986). For thermocline and early bloom populations, maximum rates of photsynthesis (P,,J are in the range 5-log C (g Chl a)-' h - ' (Pingree et al., 1976; Holligan and Harbour, 1977; Jordan and Joint, 1984; Tett et al., 1986), which are similar to those for other phytoplankton species. By contrast, within frontal blooms (Chl a >20 mg m-3), the water column becomes depleted of inorganic nutrients, values for P,,, are < 1 g C (g Chl a)-' h-I, and the population growth rate is close to zero (Holligan et al., 1984b). It appears, therefore, that nutrient depletion leads to reduced photosynthetic efficiency and a lower growth rate. Survival of the bloom must also depend on low grazing mortality. These effects, together with the vertical distribution of G . aureolum which enable the sequestration of nutrients from bottom water (Holligan et al., 1984b), provide a mechanistic explanation for the exceptional blooms of this dinoflagellate along tidal fronts (Pingree et al., 1975). The standing crop of G . aureo-

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lum can exceed 50 g C m-* (Holligan et al., 1984a), which represents a real minimal value for net primary production, assuming no horizontal accumulation (see below). Satellite observations suggest that large blooms develop in about 1 month (Holligan et al., 1983a) so that maximum rates of net photosynthesis are likely to exceed 2 g C m2-' day-' in the early stages. Indirect evidence for high rates of primary production in frontal regions comes from a consideration of the relationship between chlorophyll standing crop and photosynthetic rate. Despite the variability in photosynthetic parameters (Savidge and Foster, 1978; Videau, 1987), there is evidence for a positive correlation between biomass and production rate in stratified and frontal waters (Richardson, 1985; Videau, 1987), with daily primary productivity being determined largely by surface irradiance (Jordan and Joint, 1984; Platt, 1986). In view of the sampling problems for rate measurements, determining the distributions of chlorophyll and of optical properties may prove to be the most useful approach to assessing primary productivity in frontal regions, with blooms of dinoflagellates such as G. aureolum being treated as a special case. The inference that the high chlorophyll concentrations commonly observed at tidal fronts are indicative of high rates of production has been questioned by Le Fevre (1986), mainly on the grounds that physical aggregation within convergent circulation patterns is a more likely explanation than in situ growth. Physical accumulation mechanisms are known to be important over scales of 1 km or 1 day (Mackas et al., 1985), as is clearly evident from direct observations in frontal regions (Pingree et al., 1975). However, at scales of 1 &I 00 km (days) characteristic of the frontal blooms, biological properties (i.e. growth) are almost certainly dominant in determining phytoplankton distributions and abundance. Within the blooms, local accumulation effects associated with Langmuir cells, internal waves etc. are usually observed. Le Ftvre (1986) is also critical of the use of one-dimensional vertical models and concepts to explain algal growth in complex physical environments such as frontal regions. In both observational (Pingree et al., 1975; Holligan et al., 1984b) and modelling (Tett et al., 1986) work, this approach to considering light and nutrient availability was adopted as the best practical means for understanding phytoplankton growth in frontal ecosystems. The assumption that vertical mixing processes are, in general, more important than horizontal ones in determining nutrient fluxes is substantiated by theoretical considerations (Loder and Platt, 1985). Furthermore, no rational hypotheses based on horizontal mixing and advection to explain nutrient and chlorophyll distributions in both deep and shallow water fronts (Pingree et al., 1978) have yet been formulated. E. SPATIAL AND TEMPORAL VARIABILITY

Within the main types of physical environment on the continental shelf-

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stratified, frontal and well-mixed waters (Fig. 7)-the environmental factors that control phytoplankton growth are extremely complex. For this reason alone, it is not surprising that the range of estimates for annual primary productivity appears to be considerable, both spatially (Steele, 1956; Fransz and Gieskes, 1984) and temporally (Russell et al., 1971). The causes are both direct and indirect influences on nutrient and light availability, including the effects of wind, precipitation, river run-off and surface heat fluxes on stratification, the effects of river run-off and shelf break exchanges on nutrient levels, and the effects of sunshine and turbidity (coastal erosion, bottom mixing, rivers, etc.) on water column irradiance. For any given location, annual differences in primary production are likely to be related largely to the light environment; a more efficient utilization of nutrients, and therefore higher productivity, will result from above-average solar illumination (especially with respect to photosynthesis in mixed water columns and within the thermocline) and from longer-than-average periods of stratification. By contrast, the initial (late winter) nutrient content of the water column is rather constant (Pingree et al., 1977b) from year to year, so that differences in nutrient availability are likely to be relatively small. Blooms of the dinoflagellate Gyrodinium aureolum, within which a high nutrient input of nutrients across the seasonal thermocline is maintained by biological processes (Holligan et al., 1984b), are exceptional in this respect. The ecological significance of variations in primary productivity has not been investigated in any detail except through modelling work (e.g. Steele, 1974), although it is recognized that certain shelf areas are characterized by greater secondary productivity than others (Brander and Dickson, 1984). In particular, annual variability within a given region is poorly understood, in terms of both the relative magnitude of the effect and how it influences the food chain. This seems a rather intractable problem due to the difficulties of adequate sampling and of making appropriate rate measurements.

VI. FATE OF PLANT MATERIAL WITHIN THE SHELF ECOSYSTEM Most of the uncertainty in values of net primary production for NW European shelf seas arises from various sampling and methodological problems. Attempts to evaluate the fate of plant material in the ecosystem have led to similar doubts about the quantities of organic material produced. Such studies have ecological or biogeochemical objectives, and often include measurements of properties that relate to population taxonomy (cell size, sinking rates, pigment composition, mineral phases, storage products, etc.). There are two main conclusions from the ecological work. Firstly, in a reevaluation of Steele’s (1974) model of the North Sea food chain, Baars and

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Fransz (1984) estimated that the accepted value for phytoplankton production (-90 g C m-2 yr-I) is low by a factor of about two. This view stems partly from a consideration of new information on the energy requirements of benthic (see Wilde et al., 1986) and microheterotrophic (see Burkill et al., 1987) organisms, and partly from restrictions imposed by more realistic models of the relationship between photosynthesis and fish production (Jones, 1984). It is now recognized that the Fladen Ground in the northern North Sea, where Steele made his detailed observations on primary production, is an area of relatively low biological activity due to the prevailing physicochemical conditions in summer. But, remarkably, comparable nutrient budgets have not been undertaken for other hydrographically distinct regions of the continental shelf. There is increasing evidence for the sedimentation of a substantial proportion of the phytoplankton standing crop each year. As pointed out by Fransz and Gieskes ( 1984), conditions when the phytoplankton growth rate exceeds the zooplankton grazing rate occur regularly, and will normally result in the loss of plant material to the bottom water and sediments. This imbalance may be due either to rapid phytoplankton growth, as at the time of the spring diatom outburst, or to some inhibition of grazing as occurs within populations of colonial flagellates such as Phaeocystis (Joint and Pomroy, 1981; Joiris et al., 1982) and of dinoflagellates (e.g. Holligan et al., 1984a). Vertical fluxes of particulate material are difficult to measure in waters stirred by tides, but sediment traps have shown that large quantities of plant material do sink through the seasonal thermocline (Davies and Payne, 1984; Cadee, 1985, 1986b). Furthermore, on a larger scale, there is speculation that substantial amounts of phytodetritus may be transported from continental shelves to the continental slope (see Rowe et al., 1986). This scenario has yet to be critically examined for the NW European shelf, but the Norwegian Channel is known to be a major sink for particulate material from the North Sea (van Weering, 1981). The second ecological conclusion is that there are consistent spatial variations in primary production rates which, for the main part, are attributable to physical mixing processes and the disposition of tidal fronts. This is based on studies of larval fish (see Sinclair and Tremblay, 1984), planktonic organisms (e.g. Kisrboe and Johansen, 1986) and benthic animals (e.g. Creutzberg, 1985). In each case variations in total biomass of consumer organisms are usually associated with changes in species composition so that, on account of differences in growth efficiencies for individual species, it is not possible to relate heterotroph biomass to autotroph productivity directly. However, physiological evidence, such as that presented by Moal el al. (1985) on digestive enzyme activity in zooplankton, should resolve this problem of interpretation. The biogeochemical investigations (e.g. Lancelot et al., 1986) are less well advanced in providing quantitative information, relative or absolute, about

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rates of primary productivity. However, the types and proportions of plant products, which vary with growth conditions as well as taxonomic composition (Morris, 1981), include specific compounds that can be monitored in secondary (i.e. after death or predation) dissolved and particulate phases. Substances resistant to microbial degradation and chemical dissolution are of particular interest in this context. Examples from sediments include silica frustules of diatoms, calcite coccoliths (plates) of coccolithophores, plant pigment and their degradation products (e.g. Billett ef af., 1983), fatty acids attributable to diatoms (Smith et af., 1983b), dinoflagellate sterols (Boon et af., 1979), and coccolithophore longchain ketones (Brassell et al., 1986). In each case relative information on rates of primary production can be inferred from deposition rates and from taxonomic data-for example, diatom remains are indicative of more productive ecosystems than dinoflagellate or coccolithophore remains, at least for oceanic ecosystems (see Margalef, 1978). The dissolved products of phytoplankton metabolism are less well known due to analytical difficulties, but trace volatile substances which can be isolated from sea water and concentrated are likely also to prove valuable in this context. For example, the distribution of dimethyl sulphide, a cleavage product of the osmolyte dimethylsulphoniopropionate,is an indicator of certain types of phytoplankton (Holligan er al., 1987)and of grazing activity (Dacey and Wakeham, 1986). These marker compounds, even though they constitute only a small proportion of the total organic matter of phytoplankton, are likely to yield valuable information about variations in rates of primary production as conditions controlling their production and fate become better understood. For particulate organic matter in shelf seas affected by tidal stirring, there will always be special problems in interpreting distributional data due to the effects of resuspension. However, at least over short time-scales (i.e. days to weeks), studies on the dissolved products of phytoplankton metabolism, including volatile substances, are likely to provide important new information about the dynamics of phytoplankton growth.

VII. CONCLUSIONS Reliable estimates of the productivity of marine phytoplankton are required on a global scale for biogeochemical studies on the exchanges of materials between the ocean, atmosphere and marine sediments which play such an important role in determining the nature and stability of the global environment (Lovelock, 1986), and on a regional scale for the proper management of biological resources in coastal seas, which includes the need to predict the effects of over-exploitation and pollution on the food chain. Two basic questions arise: what controls phytoplankton growth, and what are the fluxes of materials through phytoplankton?

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For the shelf seas in general, including those of NW Europe, there has been considerable progress with the first question over the last 10-20 years. This has largely been the outcome of laboratory studies on phytoplankton growth and of field studies relating phytoplankton distributions to physical and chemical conditions in the water column. As a result, a more rigorous and objective framework has been given to the classical ecological studies completed during the first part of this century, and much of the variability in phytoplankton biomass can be explained objectively in terms of the effects of nutrients, light and grazing on species growth and succession. By contrast, progress with the second question has been slow. Estimates of net primary production for the NW European shelf are mainly in the range 50-300 g C m-? yr-’, and are based on various methods and assumptions. Although there is some consistency in the results, with the lower values for strongly stratified or highly turbid waters and with a degree of compatibility between different sets of observations, a rational analysis of either spatial variability in mean annual net primary production or of annual variability for a given location is still not possible. Thus for practical purposes there appears to have been little advance since the pioneering work of Steele (1956), with the exception of a better understanding of phytoplankton growth in coastal water areas as a result of multidisciplinary investigations (e.g. Joiris et al., 1982). There seem to be two reasons for this situation. First, far too much reliance has been placed on a single investigative method, incubation experiments with I4CO2, that gives results which are difficult to interpret in a physiological sense (i.e. the distinction between gross and net photosynthesis) and from which there is no dependable way to extrapolate in space and time. Secondly, biologists have made little use so far of new information about physical mixing processes in tidally stirred shelf seas. The latter is particularly surprising since Steele’s original computations depended on the parameterization of nutrient fluxes due to mixing across the seasonal thermocline and, furthermore, the results of 14C02and O2 measurements were used to check the validity of the phosphate production model. A fresh start therefore seems necessary, which not only incorporates recent concepts about nutrient regeneration and fluxes across the seasonal thermocline (the importance of both processes was clearly stated by Steele), but also makes use of the physical framework provided by tidal mixing models (Pingree, 1978b). Although the significance of the frontal boundaries in relation to plankton productivity remains controversial (Le Fevre, 1986) they d o represent predictable boundaries to distinct plankton communities in mixed and stratified shelf waters which have quite different, but as yet poorly defined, dynamic properties. In ecological terms, various causes of variability in plankton distributions are recognized. Climate has profound effects on the availability of light and nutrients to phytoplankton. In both mixed and stratified waters of the NW European shelf, significant annual differences (e.g. Maddock et al., 1981) and

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longer term trends (Reid, 1978; Robinson and Hunt, 1986) are found in both the species composition and total abundance of natural populations. Various hypotheses to explain the trends in relation to climate have been proposed (Southward, 1980; Radach, 1984; Colebrook and Taylor, 1984; Colebrook, 1986). Even more intriguing is the possibility of feedback effects on climate due to the release of volatile organic compounds by phytoplankton (Charlson et al., 1987). There are also changes due to human activities, particularly in response to nutrient discharges from rivers (Postma, 1978, 1985; Radach and Berg, 1986). In coastal waters, at least, these have affected phytoplankton distributions (Hickel et af. 1986) and led to increases in primary productivity (Cadee, 1986a). Against this background of variation and change, what is the best way of obtaining a more reliable and definitive account of primary production for the NE European shelf seas? “Baseline” studies based on restricted sets of observations using a single method such as I4CO2uptake will never suffice. One possible approach is through experimental ecophysiological work on the dominant species/taxa in the annual succession to define growth requirements and characteristics, in parallel with the development of rational models of phytoplankton productivity for realistic ecological (Fasham, 1985) and environmental (Taylor et al., 1986) situations. A combination of observational (including remote sensing) and experimental (using various methods) work at sea over appropriate time- and space-scales would allow the models to be objectively evaluated. However, for various practical reasons, a more effective approach is likely to be an extension of the nutrient budget method of Steele (1956) to include mixed and frontal, as well as stratified, waters. Nutrient analyses, giving continuous profiles (vertical and horizontal) of phosphate and nitrate, can now be used routinely on ships. Furthermore, with new information about the determinant physical, chemical and biological processes, rates of nutrient regeneration in the water column and sediments, and of nutrient exchange at boundaries (thermocline and fronts, as well as land-sea and sea-sediment interfaces) can be estimated more reliably. Specific problems such as the turnover of dissolved organic material or variations in the chemical composition of growing cells can be investigated experimentally. Also, as shown clearly by Steele (1956), the general problem of interannual variability appears tractable from a consideration of vertical mixing, although in a broader geographical framework the significance of horizontal advective fluxes may prove difficult to assess. It will not be an easy task to make a reliable and accurate description of phytoplankton productivity in the shelf seas of NW Europe, but the benefits for management problems and predictive purposes relating to future uses of these seas would be very considerable.

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416.

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AUTHOR INDEX

A Abbot, M . R.. 244,248 Abdullah, 71 Abreu-Grobois. F. A,, 19.48 Adair. W . S.. 56. 88 Adams, A. B.. 172. 173. 185 Adams. V. D.. 172. 173. 185 Adam. Y.. 248 Aderkas, P., von. 75.93 Admiraal, W., 224, 226, 230. 243. 251 Agoumi. A,. 21 7.232.234.243 Ahmed. S. I.. 244 Aiken. J . . 200. 243. 246. 250, 251 Al Araji. Z. T.. I7,48 Aldrich. H. C.. 67. 88 Alizai. S. A. K.. 145. 188 Allen. G. P.. 145, 185 Allen, J. R. L.. 104. 126, 129. 142, 143. I85 Allison, P. A., 142, 185 Alvin, K . L.. 176. 185 Ambard-Bretteville. F., 52 Amos, D. H.. 178. 187 Andersen, K . P., 194, 25 I Anderson, D. M . . 226.246 Anderson, J . A. R., 150, 185, 186 Anderson. R., 10, 31.48, 50 Anderson, A,, 123, 186 Anderson, E., 67,88 Anderson-Kotto. I., 87, 88 Andreae, M. O . ,243 Appleby, R. S., 10, 12, 51 Araki, S., 32, 34, 48, 50 Arao, T., 34,35,48,50 Arnold, M. K., 131, 188 Ashton, N. W., 90 Auling, G., 35,48 Austin, R. W., 203,243 Axelrod, D. I., 151, 186 Azarn, F., 21 1.243

253

B Baars. M . A,, 238,243.245 Baasch. K . H.. 52 Baeyens, W., 225,243.248 Bailay, R . W.. 92 Bajon-Barbier, C.. 60, 88 Baldwin, M., 72, 77,91 Bannister. T. T., 208. 209,247 Banse, K . . 197, 217, 243 Barber. J., 49 Barbier. C.. 60, 88 Barghorn, E. S.. 177, I88 Barmeier. J . C.. 189 Barrnett. R. J.. 45.46.47. 50, 51 Bartels, C. T., 44,48 Basaraba, J., I86 Bashe, D., 93 Bauer, L., 73, 74, 75, 88 Bearce, S. C., 187 Beardall, J., 194. 204, 245,249 Beck, J. C., 45.48 Bednara, J . , 69,92 Bell, E., 89 Bell, P. R., 59-93 passim Bellan, I., 200, 243 Beltz, C. K.. 68,90 Ben-Amotz. A., 47,48,49 Bennekom, A. J. van, 194,251 Benninghoff, W. S.. 108, 187 Benoit, R. E., 122. 186 Benson. A. A,, 2, 13.45,48,49 Bentley. D., 243 Berg. J., 242, 249 Berguis. E. M., 251 Berkaloff, C., 48 Berman, F., 248 Berman, T., 244 Berner, P., 250 Berrie, G. K., 75,89 Berry, E. W., 128, 186

254

AUTHOR INDEX

Bertels, A,, 214, 247 Berthois, L., 121, 186 Bessereau, G., 187 Bhardwaja, T. N., 71.89 Bhatnagar, A. K., 64,69,90 Bhatnagar, S. P., 63, 67.90,91 Billen, G., 226. 232, 247 Billett, D. S. M., 210, 240, 243 Billyard, T. C.. 48 Binelli, G., 92 Bird, E. C. F., 143, I86 Bird, J., 92 Birrien, J. L., 251 Bishop, D. G., 50 Bisseret, P., 48 Blasco, D., 209,243 Blecker, H . H., 50 Bligny, R., 52 Bloch, K., 50 Block, R. J., 10,49 Boalch, G. T., 197, 231, 232. 234,235, 243,248 Bolton, P., 7,48 Bonnevie-Svendsen, C., 99, 186 Boon, J. J., 240,243 Borowitzka, L. J., 20,48 Boschetti, A,, 10,49, 5 I Bose, A., 246 Bossard, P., 250 Bossicart, M., 247 Botkin, D. B., 252 Bowen, C. C., 90 Bowers, D. C., 219,250 Bowman, M. J., 222,227,228.243 Braarud, T., 197,243 Brack-Haynes, S. D., 177, 186 Braithwaite, A. F., 71, 89 Brander, K . M., 194,232,238,243 Brassell, S. C., 240, 243 Braten, T., 58, 89 Brawley, S. H., 58, 59, 89 Bray, J . R., 99, 186 Bredemeijer, G., 186 Bressler, S. L., 244 Brett, D. W., 189 Breuer, J., 51 Brewer, P. J., 215,243 Bridge, J . S., 126, 186 Broadwater, S. T., 59,65,89 Brockmann, U . H., 223,232,243 Broenkow, W. W., 245 Brown, A. D., 20,48 Brown, A. E., 4, 10,33,48

Brown, B. O., 245 Brown, J. W.. 245 Brown, R. C., 65,89 Bryan, G. S., 64, 89 Bryan, G. W., 40.48, 53 Bryan, J. R.. 213. 243, 251 Bryce, T. A., 9.48 Brylinski, J . M . . 222. 243 Burgeff, H . , 75. 89 Burkill. P. H., 226, 239, 243. 248 Burnham. R. J., 105. 128. 167. 168. 181. 183, 186. 190 Burris, J . E.. 204. 243 Burris, N., 53 Bustin, R. M., 143, 145, 146. 190 Butler, E. I . , 206. 207,224. 225, 243, 245. 249,250 Butler, R. D., 59. 92

C Cadee, G . C.. 232.239.242.243 Callow, J . A,, 90 Callow, M. E.. 90 Camefort, H., 64. 89 Campbell, J. W., 250 Camus, P., 246 Canul, R.. 186 Carey, S. N.. 153. 186 Caron, L., 32.48 Carothers, Z . B., 60,90,93 Carroll, S. M., 187 Casadevall, T. J.. 154, 191 Casagrande, P. J., 190 Cave, C. F., 62,89,92 Cawood, A. H., 93 Chaloner, W. G., 166, 176, 180, 186, 189 Chamisso. A., von, 55,93 Champagne-Philipe, M., 246 Chaney, R. W., 179, 186 Charlson, R. J., 242,243 Chiang, K. G., 83,93 Cho, S. H., 24, 27.48,49, 53 Choudhury, M. K., 49 Christiansen, R. L., 153, 186 Clark, D. K., 245 Clarkson, D. T., 38,40,49 Clayton, J. R., 244 Cleveland, J. S . , 244 Cleve, P. T., 196 Clift, R., 104, 186 Cochems, N., 49 Codispoti, 21 5 Coffin, 1 14, 118, 157

AUTHOR INDEX

255

DeMaggio. A. E., 84, 89 Cohen, A. D., 190 Colebrook. J. M., 198,210,227, 242, 243 Denman, A. W., 217,249 Coleman. J. M.. 143. 150, 186 Denman, K . L., 248 Colijn. F., 25 I Dessort, D., 48 Collinson, M. E., 117, 118, 124, 125, 186 Devol,A. H., 191,207,213,247 Collos, Y ., 207. 208. 243. 244, 250 Dickinson, H. G.. 67,68, 69, 82,85, 87, Conn, E. E.. 13,45, 53 88, 89.9 I , 92,93 Conway, D. V. P., 225,226,251 Dickson, R. R.. 194,232,238,243 Coombs, J. L.. 47.49 Diel, S . , 225, 226,244,245 Cooper, L. H . N.. 212,213,244.246 Diers, L., 60, 89 Digby, L., 71,90 Corner. E. D. S., 207.210.21 I . 244 Correns, C.. 85. 89 Dilcher, D. L., 104, 13I , 189 Correns. C. W., 177, 186 DiMichele, W. A,. 178, 189 Cottrell. J. C.. 25 I Dittus, W. P. J., 110, 186 COVC.D. J . . 90 Dixon, P. S.. 197. 248 Covington. D.. 143, 186 Dohler, G.. 20,49 Cowles. T., 244 Dokulil. M., 250 Crabbcndam. K. J . . 56.89 Dopp, W., 70, 7 I , 89 Craig, H .. 2 15. 244 Dorf, E., 151, 186 Craighead. F. C.. I 10. 186 Dortch, Q., 208, 244 Crcbcr, G. T., 166, 186 Doucc. R.. 13. 14. 34, 3 5 4 6 , 52 Crepet. N . L.. 130. 186 Doue, R., 50 Creutzbcrg. F.. 236,239.244 Douglas, D., 246 Cross. A. T.. 174, 186, 190 Douglas, D. P., 187 Cullen. J. J., 247 Douval. J. C.. 52 Cummins. K . W., 106, 123, 186, 189 Doyle, J., 65.69, 70,90,91 Cuneo, R.. 181, 186 Doyle. W . T., 90 Cunningham. C.. 246 Drebcs, G.. 197, 244 Curtis. P. J., 248 Dring, M. J.. 194, 204, 214,244, 246 Droop, M. R., 207,208,244,251 Cushing, D. H . . 196.216.225,235,244 Cutter, E. G., 90 Drum, R. W.. 177, 186 Dubaca, J. P., 48 Dubacq, J. B., 52 D Dacey, J . W. H., 240.244 Dubinsky, Z., 203, 204,244,245 Dagg. M., 21 I . 244 Duckett. J. G., 58, 59, 62, 89.90, 92 Ducklow, H . W., 212,244 Daghlian, C. P..130, 186 Daniel, J. Y.. 248 Duffield, W. A,, 160, 186 Dannell, G. S., 123, 186 Dugdale, R. C., 195,207,208,210, 213, Darley. W. M.. 49 244 Daro, M. H., 226,244,247 Dunstan, W. M., 206, 250 Datz. G.. 20,49 Dunwiddie, P. W., 108, 166, 173, 186, Davies, A. G., 207,210,21 I , 224, 244 187 Davies, C. L., 10, 51 Dupont, J., 243 Davies, J . M., 2 14,225,239,244 Dupouy, C., 246 Davis, P. G., 244 Durand, B., 145, 187 De Bock, P., 117, 187 Dzurisin, D., 166, 191 De Vries, H . , 123, 186 Deane, E. M., 50 E Ebel, F., 105, 187 Decadt, G., 243 Dedeurwaerder, H., 243 Edmonds, R. L., 108,187 Edwards, A., 202,251 Degges, C. W., 187 Dehairs, F., 243 Efremov, I . A., 97, 187 Delwiche, C. C., 252 Egan, B., 245

256

AUTHOR INDEX

Eggert, D. A., 177,188 Eggler, W. A,, 172, 187 Egglisher, H. J., 106, 187 Eglinton, G., 243, 250 Egmond, P., van, 92 Ehrensberger, R., 77,90 Eichenberger, W., 5,6, 10, 1 I , 13,22,33, 45,46,47,49, 5 I , 52 Eilertson, H. C., 234,244 Ekberg, I., 88 Elmore, H. W., 75,90 Elovson, J., 4, 10, 33,48,49 Elwood, J . W., 189 Eppley, R. W., 195, 197,202, 207, 208, 209,212,213,216,223,244,246 Erga, S. R., 234,244 Eriksson. G., 88 Erwin, J., 50 Esaias, W. E., 243,250 Estep, K . W., 197,244 Ettl, H., 70, 72, 80,90 Evans, J., 49 Evans, L. V., 73,90 Evans, R. H., 245 Evans, R. I . , 64, 89 Evans, R. W., 20,22,23,49 Evans, W. D., 178, 187 Eyme, J., 65,90 F Falkowski, P. G., 202, 204, 244,245, 246,250 Farmer, J. B., 71,90 Fasham, M. J. R., 200,202,204,2 17, 245 Fattom, A., 51 Fay, P., 50,90 Feige, G. B., 2, 13, 14,49 Feliciano, J. M., 178, 187 Fenchel, T., 243 Fergson, 117 Ferguson, D. K., 104, 105, 106, 107, 108, 109, 110, 112, 113, 117, 123, 124, 144, 171, 187 Ferguson, R. L., 207,245 Ferrari, R. A,, 45,48,49 Field, J. G., 243 Fisher, S. G., 113, 187 Fisk, L. H., 151, 187 Floodgate, G. D., 245 Flynn, K . J., 207,224,245 Fogg, G. E., 197,204,214,226,236,245 Foley, A. A.,7,49

Folkard, A. R.. 221,247 Forest, C. L., 58.90 Fork, D. C., 18.49 Forster, G. R., 249 Foster, P., 223,224, 235, 237, 245, 250 Fowke. L. C., 71,90 Foyn, B. R., 82.90 Francis, J . E., 166, 187 Franks, R., 84,90 Fransz, H. G., 225, 231,232. 233.238. 239,243,245 Fraser, C . J.. 185 Freeberg, J . A,, 76.90 Frentzen, M., 34.49 Fried, A., 22.49 Fritz, W. J., 157, 162, 163. 164. 165. 187. 188

Froggatt, P. C.. 155. 187 Frost, B. W., 210.21 I . 245,250 Frova, C.. 92 Fuhrman, J. A., 207.245 Furuya, M.. 5, 10, 22. 33. 52 G Gaarder, K . R., 197,246 Gabarajeva, N. I., 66.90 Gachter, R., 250 Gadow, H., 172, 187 Gagliano, S. M., 186 Gallagher, J. L., 145, 187 Gallegos. C. L., 249 Garrett, C., 248 Garside, C., 207. 213,245 Gastaldo, R. A., 103, 122. 128, 129. 133, 142, 144. 145, 146-147, 148, 180, 182, 187 Gastony, G . I., 81, 90 Gauzens, A. L., 250 Geider, R., 250 Geiger, N. S., 171, 188 Gerber, A., 1 I , 47,49 Gerlach, S. A., 223,245 Gieskes, W. W. C., 214, 225, 231,232, 234,238,239,245,251 Gifford, E. M. jr., 68,93 Gilbert, G. K . , 133, 187 Gilbert, P. M., 245,247 Gilbert, V. C., 110, 186 Ginzburg, B.-Z., 49 Ginzburg, M . , 49 Girty, G. H., 187 Given, P. H., 190 Gjems, O., 99, 186

AUTHOR INDEX

Glicken, H., 190 Goebel. K., 75. 90 Goering, J. J.. 195. 244 Gocyens, L., 243 Goldman. J. C.. 202, 207. 208. 209,2 12, 2 15.2 I6,243.245.246,247 Goodenough. U . W., 58.91 Goodsalk, G. L., 189 Gordon. H. R . . 216,245 Goreham. E.. 99, 186 Gosse, P.. 243 Gottesman, S., 80, 90 Could. H. R.. 142. 187 Gounaris. K., 2. 13. 32,45.49 Grace. J. R.. 186 Graham.A.. 151. 187 Graham. L. E.. 56. 57. 65. 90 Gran. H. H., 196 Grant. P.. 190 Gray. J . S.. 243 Greer.A.C.. 114. 117. 119. 120. 121. 125, 138, 190 Gregson. B. P., 191 Crier, C.. 108 Griffiths, D.. 245 Griffiths, D. K.. 219,220,249 Griffiths. G.. 28.49, 53 Grimley. N . H.. 80. 90 Groom, S., 220 Gros, P.. 232, 245 Grot, A. V., 49 Guest, K . P., 214, 246 Gulliksen, 0. M . . 90 Gurr, M . I., 44,45,46,49 Gusev, M . V.. 20,49

H Hafsaoui. M., 249 Hagberg, A.. 90 Hagberg, G., 90 Hague, A., 151, 187 Haines, T. H., 10,49 Hall, K . C., 49 Halpern, C. B., 172, 187 Hamazaki, Y., 51 Hanlon, R. D. G., 124, 188 Hann, A. C., 53 Hansen, V. Jr., 194, 250 Harbour, D. S.. 197, 198,235,236,243, 246,248 Hargraves, P. E., 244 Harmon, M. E., 172, 187 Harrap, R., 246

257

Harris, G . P., 196, 245 Harris. J. R . W.. 251 Harris, P., 49, 51 Harris, R. P., 224, 226, 245. 246 Harris, R. V., 42,43,44,49, 51 Harris, T. M.. 176, 188 Harrison, J. D., 51 Harrison, S., 163, 164, 187, 188 Harrison, W. G., 195. 196,204, 207. 209, 2 1 I , 2 13. 2 15, 230. 244, 245, 246, 249 Hartley, B.. 197, 246 Harvey. H. W., 196,212,246 Harwood. J. L., 3-53 passim Hasclkorn. R., 13. 50 Hassell, P. R., van, 53 Hauflcr, C. H.. 93 Haugen. E. M., 197,248 Hayward, T., 21 5,244 Head, P. C.. 246 Head. R . N.. 205,246,249 Heaney, S. I., 209, 246,25 I Heath. G. W., 131, 188 Heath, M . R.. 249 Hegeman. J., 232,243 Heilbronn. A,. 76, 90 Heimdal, B. R., 197, 209, 234, 243, 244. 246 Hein, E., 50 Heinemann, B., 249 Heinemam, K., 248 Heinemann, K . R.. 251 Heinen. W., 186 Heinroth, L., 226,247 Heinz, E., 34,48,49. 52. 53 Henderson, E. W., 199,250 Hendrix, L. B., 172, 188 Hepler, P. K., 63,91 Herbert, D., 247 Herd, Y. R., 66,90 Heslop Harrison, J., 67,68, 77, 82, 83, 89,90,91 Heymann, V., 244 Hickel, W., 242, 246 Hickey, L. J., 191 High, L. R., 131, 189 Hirsch, A. M., 75, 90 Hitchcock, C., 6, 14, 45, 50 Hitchcock, G . L., 214,246 Hobday, D. K., 150, 188 Hobson, L. A., 214,246 Hoffman, L. R., 58, 59,90 Hofmeister, W., 56, 90

258

AUTHOR INDEX

H~jerslev,N. K., 221, 223, 246 Holcomb, R. T., 191 Holligan, 197-249 passim Holm-Hansen, O., 49 Holton, R. W., 18, 50 Holt, V. I., 186 Holyoak, D. T., 143, 188 Holzer, G., 53 Homan, W. L., 92 Hopkins, A. W., 65,90 Horne, E. P. W., 247 Horner, H. T., jr., 65,68,90 Horvath, I., 53 Horwood, J. W., 201,217,234,246 Howard, F. O., 186 Howe, S., 244 Howland, R. J . M., 248 Howling, D., 42,44. 50 Hsia, Y., 191 Hulanicka, D., 12, 50 Hulbary, R. L., 65,90 Hummerstone, L. G., 40,48 Hunter, J. R., 150,242,218,250. 251 Hunt, H. G., 250 Hunt, J. W., 188 Hunt, R. J., 187 Hushovd, 0.T., 78.90 Hutchinson, D. E., 131, 188 Hyams, J. S., 92 Hynes,H. B. N., 105, 106, 122, 124, 188

I Ichimura, S., 247 Iddings, J. P., 187 Iijima, N., 50 Iler, R. K., 177. 188 Mias, Z. M., 77, 90 Ingram, L. O., 20, 51 Ito, S., 48 Itoh, S., 91 Izmailow, R., 72,90 J Jackson, G. A., 206,2 10,2 1 I , 246 Jacob, N. J., 248 Jacobson, D. M., 226,246 Jalouzot, M.-F., 70,90 James, A., 205,246 James, A. T., 26,43,45,48,49, 50, 51 Jamieson, G. R., 28,38,50 Janda, R. J., 161,188,191 Janero, D. R., 45,46,47, 50 Janzen, D. H., 105,188

Jaworski, J. G . , 17, 53 Jayasekera, R. D. E., 79.90 Jefferson, T. H.. 164, 165, 177, 188 Jelsema, C. L., 46, 50, 51 Jenkin, P. M., 2 13,246 Jenkins, W. J., 246 Jensen, K. G., 65.90 Jensen, W. A.. 64.69. 92.93 Jernik. J., 105, 188 Jewson, D. H., 194,203.204.214.244. 246 Jobson, S., 91 Johansen. K., 239.247 John, A. W. G., 249 Johnson, K. S., 215.246 Johnston, R., 223.246 Joint, I. R., 197. 198. 201.212.222. 226. 227.23 I , 232.234. 236. 237, 239. 247.25 1 Joiris, C:. 194. 212,214. 231, 239, 241, 247 Jones, A., 246 Jones, A. L., 3, 28, 30, 32. 33, 34, 35. 39, 40,41,42,50,51 Jones, D. A,, 245 Jones, K., 25 I Jones, K. J., 247 Jones, P. G. W., 223,246 Jones, R., 194, 236,239,247 Jopling, A. V., 133, 134, 188 Jordan, M . B.,227,234,236,237,247 Joyard, J., 13, 14, 34, 35.46, 50 Judkins, D., 244 Jupin, H., 48 Juszko, B. A.. 248 K Kahng, S. H., 214,250 Kames, W. H., 142,188 Kana, T. M., 204,247 Kapil, R. N., 64,69,90 Karowe,A. L., 164, 165, 177, 188 Kasha, K. J., 77,90 Kassab, J. Y., 245 Kates, M., 10, 1 I , 13, 20, 21,45,48,49, 50,52 Kaur, D., 63,90 Kaushik,N. K., 122, 123, 124, 188 Kawaguchi, A., 7, 10,35,48, 50 Kawalczewski, A., 124, 188 Kayama, M., 28,50 Kelley, B. C., 65,90 Kelly, W., 51

AUTHOR INDEX

Kenrick, J. B., 9, 50 Kenyon. C.N., 7, 14,20,50 Kermicle, J. L.. 77, 90 Khalanski, M., 243 Kidston, R., 151, 188 Kieffer, S. W., 153, 188 King, F. D., 202,207.208.210,213,247 Kiorboe, Th.. 239. 247 Kirk, T. 0..203.247 Kishino, M., 203, 247 Kleiffer, 153 Klein Breteler. W. C. M., 226,244 Kleppinger-Sparace, K. F., 13, 51 Klis, F. M.. 89, 92 Klug. M. J., 186 Knoll, A. H., 177, 188 Knowlton. F. H.. 187 Knox, R. B.. 77.91 Knox. S . , 243 Kojan. S., 93 Kok, A,, 25 I Konar, R. N.. 64.77.91 Koutsikopoulos, C.. 248 Kraay, G. W., 231,232.234.245 Krassilov, V. A , . 99, 188 Krespki, W. J.. 19, 50, 51 Kuiper, P. J. C., 53 Kuligowski-Andres. J., 93 Kumari, L.. 83,91 Kummel. F., 187 Kuparinen. J., 214. 247 Kuroiwa, T.. 91 Kwa, S. H., 75, 91

L La Rue, C. D.. 77.91 Laccadena, J.-R., 77.91 Laird, S., 71,91. 93 Lal, M., 59, 60, 73,75, 79, 81,91 Lambein, F., 9, 13, 50 Lampitt, R. S., 243 Lancelot, C., 226,232,239,247 Landriau, G . , Jr., 248 Lang, W. H., 75,91,I5l, 188 Lange, F. de, 75, 151,243 Larsen, D. W., 171, 188 Laur, M.-H., 2, 30, 52 Laurier, D., 185 Lavin-Peregrina, M. F., 249 Laws, E. A,, 208,209,247 Lawton, E., 75,91 Lazarenko, A. S., 73, 82,91 Lazaroff, N., 56,91

259

Le Caro, F., 1 13, 188 Le Corre, P., 248, 25 1 Le Coz, J. R., 248 Le Fevre, J., 219,237, 241, 247, 248 Lebour, M. V.. 197,246,247 Lee, A. J., 217, 221, 247 Lem, N. W., 16,17,50 Lemmon, B. E., 65,89 Lennon, H. J., 225,250 Leo, R. F., 177, 188 Lenten, N. R., 90 Lesnyak, E. N., 91 Levine. R. P., 45,48 Lewis, D.. 88, 89 Lewis, M. R., 194,207,246.247 Li, F. L., 67,91 Li, W. K. W.,209,216,247 Liddicoat, M., 243 Lien, S., 53 Lignell, A,, 40, 50 Likens, G. E., 113. 187,252 Lindahl, O., 226. 247 Linley. E. A. S., 226,246.248 Linscheid, M., 53 Lipman, P. W., 152, 188 Llewellyn, C. A., 197, 243,248 Lochte, K.. 226,245,247 Loder, J. W., 207.218,229,237,248 Loeuw, J. W. de, 243 Loh, C. S.,91 Lohmann, H., 196 Longman, K. A., 105, 188 Looby, W.J.. 69.91 Lorenzen, C. J., 197,2 1 I , 2 16,248,25 1 Lovelock, J. E., 240, 243, 248 Lucas, M. I.. 246 Luhr, J. F., 191 Lynch, D. V.. 22-24,25,26,50,51 M McBride, G. E., 65,90 McCabe, P. J., 148, 149, 150, 15 1, I88 McCarroll, S. M.. 187 McCarthy, D. G . ,245 McCarthy, J. J., 207, 248,250 McConchie. C. A., 63,91 MacGinitie, H. D., 132, 188 MacGregor, M., 122, 188 Mackas, D. L., 219,237,248 Mackenzie, A., 83,90 MacLeod, N. S., 191 Mcmanns, T. T., 52 McManus, J., 145, 188

260

AUTHOR INDEX

McQueen, D. R., 137, 188 Maddock, L., 201,227,232,242,248, 249 Mahlberg, P. C., 72, 77,9 I Mainx, F., 72. 91 Malej, A,, 224, 226, 245 Mamay, S. H., 177, 188 Manko, Yu. L., 172, 188 Mankura, T., 50 Manny, B. A,, 186 Manton, I.. 75. 81, 82,91 Mantoura, R. F. C., 197,243,248 Mantz, P. A,, 121, 188 Mardell, G. T. M.. 219,246,249 Margalef, R., 200. 240, 248 Marlow, I . T., 243 Marra, J., 204,248, 251 Marsden, C. R., 72,91 Marshall, S. M., 213,248 Martin-Jezequel, V., 222, 248, 249 Martin, N. C., 58,91 Martinson,. H . A,, 188 Mascarenhas, J . P., 78,84,90,93 Mathews. C . P., 124, 188 Mathot, S., 247 Megard, R. O., 194,215,248 Mehra, P. N., 75, 81, 83, 91,92 Mendiola-Morgenthaler, L., 47,51 Menon, M. K. C., 73,91 Mercer, E. I., 10, 13, 51 Meyer-Reil, L. A., 243 Miall, A . D., 126, 184, 188 Michaels, A. S., 46, 50, 51 Michel, H. P., 49 Millay, M. A., 177, 188 Miller, C. C. J., 90 Miller, J. A., 48 Mitchelson, E. G., 221, 248, 249 Miura, Y . ,52 Moal, J., 239,248 Mogensen, H . L., 63,91 Mohy-Ud-Dhin, M. T., 19, 51 Moitra, A., 64,67,91 Molder, M., 67,92 Mommaerts, J. P., 215. 220,243,247, 248 Moore, T. M., 13, 33, 51 Moorhouse, R., 45,51 Morel, A,, 203, 248 Morel, G., 75,91 Morgan, J. P., 142, 188 Morin, P., 224,248 Morley, R. J., 150, 189

Morris, I., 202, 240, 248 Morris, L. J., 43, 44, 50, 51 Morris, R. J., 250 Moshiri, G. A., 189 Mudd, J . B.. 13,45. 51, 52, 53 Mueller-Dombois, D.. 172. 190 Miiller, D. G., 81,90,91 Muller, J., 150. 186 Mullineaux, D. R., 152. 188 Murata, M..2,7,9, 13. 14, 15, 16. 17. 18, 19, 23. 34, 52 Murata. N., 48.49, 51. 52 Murphy, L. S., 197.248 Musgrave, A., 89.92 Myles, D. G.. 63, 79.91

Iv Nakamura, S.. 79.91 Nemoto, Y.. 52 Neumann, K.. 90 Nevissi, A. E.. 191 Newbold. J . D., 124. 189 Newell, R . C., 226. 246. 248 Nichols, B. W., 6, 10. 12, 14,44.45,48. 50, 5 1. 52 Nichols, J. H., 246 Nijs, J., 247 Nikitina, K . A,, 49 Nishida, I., 7, 9, 13, 14, 15, 19, 51 Nodby, O., 90 Nolan, K. M., 188 Norman. H. A., 5. 24,25. 26-27. 33.47, 51,53 Norstog, K.. 63. 77,91 Nusch, E. A,, 250 Nygren, A,, 72,91 Nykvist, N., 122, 189

0 Oakey, N. S., 247 Ohnishi, J., 35, 51 Okami, N., 247 Olesens, N. J. P., 247 Olson, G. J., 20, 51 Omata, T., 14,48,51 Onore, M., 50 Ooya, N., 76,91 Oren, 20 Orr, A. P., 213,248 Ostenfeld, C. H., 196 Ottaviano, E., 92 Otto, G. H., 100, 189 Oudin, J. L., 187

26 1

AUTHOR INDEX

Overton, E., 56,92 Overton, J. B., 73, 92 Owens, J. N.. 67,92 Owens, N. J. P., 228,243,247,248 Ozaki. K.. 126, 189 Ozer. J., 248

P Paasche, E., 209,248 Padan. E.. 51 Paerl. H. W.. 205,248 Palta, H. K.. 75. 92 Pang, Y. H., 121, 189 Paolillo. D. J., jr., 65, 92 Parke. M.. 197,248 Parker. W. C.. 189 Parrish. J. T.. 105. 124, 129. 176, 182, 183, 189. 190 Parry. D.. 92 Parson. M . J.. 92 Parsons. T. R.. 197.25 1 Partensky. F.. 236.248 Pashuk. C . T..91 Paync. R. E., 220. 225.239.244.248 Peavey. D. G.. 245 Pederson. M., 50 Pederson. S. M.. 249 Peebles. M . W., 187 Peel. M. C., 58.92 Pennell, R. I., 62,63,64,67. 69, 78,85, 87.89.92 Pennycuick, L., 219. 233, 234, 249 Peppers, R. A., 189 Pcsch, R.. 53 Petersen, R. C., 123, 186, I89 Peterson, B. J., 207, 212, 213, 214, 223, 244,248 Peterson, D. W.. 153, 186 Pettitt, J. M., 66, 68, 87, 88, 92 Pettitt, T. P., 50 Pettitt, T. R., 2, 3, 7, I I , 12, 30.31, 32, 35, 37,51 Petzold, T. J., 203,243 Pfefferkorn, H. W., 112, 143, 146, 183, 190, 191 Pflaumann, U., 243 Pham-Quang, L., 2,30,52 Philipson, M., 86,92 Phillips, T. L., 177, 178, 189 Phinney, D. A., 250 Picard, M. D., 131, 189 Pichot, G., 248 Pickett-Heaps, J. D., 58, 59, 71,90,92

Pickmere, S. E., 78,92 Pierson, T. C., 161, 189, 191 Pingree, R. D., 196-249 passim Piorreck, M., 20, 52 Pipe, R. K., 197,201, 247 Platt, T., 195, 196,202,204,209,213, 2 15,2 17, 2 18,227, 229, 230,237, 245,246,247,248,249,250 Plumley, F. G., 145, 187 Pobiner, 89 Pohl, P., 5,6, 12, 28, 38, 52 Pohlheim, F., 86,92 Polack, W., 150, 189 Pomroy, A. J., 198, 2 12,222, 23 I , 232, 234,239,247,248 Pond, V., 93 Ponzelar, E., 49 Porter, E. K., 67,92 Postma, H., 222,223,224,232,242,249 Potonie, H., 112, 189 Potter, F. W.. 130, 189 Potter, U., 67,69,85, 89 Poulet, S. A., 224,249,252 Praeger, R., 1 17, 189 Preisendorfer. R. W., 203,249 Prestegaard. K. L., 191 Pringsheim, N., 73,92 Pugh. P. R., 245,246.249 Purdie, D. A,, 244,246, 251 Pytkowicz, R. M., 246

Q Quatrano, R. S.. 89 Queguiner, B., 224,249

R Radach, G., 196, 198, 199,217,227,242. 246,249 Radunz, A,, 53 Raghaven, V., 84,92 Rai, H., 250 Raine, R. C. T., 215,249, 251 Ramsay, H. P., 65,92 Rau,G. H., 108, 109, 123, 132,189 Raven, J. A., 194,204,249 Raymond, A., 143, 184,186,189 Rebeille, F., 40, 52 Redfield, A. C., 206,212,249 Rees, E. 1. S., 245 Reid, E. H.,28, 38, 50 Reid, J. L., 21 5,250 Reid, P. C., 198, 199, 232,235, 242,249

AUTHOR INDEX

262

Reiners, W. A,, 252 Rember, W. C., 132, 151, 190 Remy, R., 7, 52 Renger, E. H., 244 Retallack, B., 59,92 Retallack, G. J., 178, 189 Rex,G. M., 121,122, 176, 177, 178,179, 180, 189, 190 Rhamstine, E., 77,91 Rhodes, E. G . , 145,189 Rice, A. L., 243 Rich, F. J., 132, 189 Richards, P. W., 113, 189 Richardson, K., 204,206,214,235,236, 237,249 Richardson, P. J., 108, 189 Rick, C. M., 93 Ridley, H. N., 117, 189 Rietema, H., 70.92 Rijpstra, W. I. C., 243 Riley, G. A., 21 3, 250 Riley, J. P., 243 Ripetsky, R.T., 75,92 Rippka, R., 50 Risk, M. J., 145, 189 Robert, D., 64, 92 Roberts, J. K. M., 49 Robinson, G . A., 198,242,250 Robinson, H. P., 49 Rodkiewicz, B., 69,85,92 Roessler, P. G., 47, 52 Rolfe, W. D. I., 189 Roman, M. R., 21 1,250 Romanov, V. V., 150, 189 Roomans, G. M., 50 Roth, J. L., 104, 131, 189 Rothwell, G . W., 177, 189 Roughan, G., 32,34,52 Roughan, P. G., 31,52 Rowe, G. T., 239,250 Rowlands, C., 49 Rudd, R. L., 113,188 Rullkotter, J., 34, 52 Runnegar, B., 100, 190 Russell, F. S., 234,238,246 Russell, N. J., 3, 50 Russell, S. D., 63,92 Ryckaert, M., 232,245 Ryther, J. H., 206,216,250 S

Sado, T., 50 Safford, R., 45,52

Sager, G., 218,250 Sager, R., 79,92 Saint John, H., 173, 190 Sakamoto, M., 214,250 Sakurai, T., 48, 50 Samain, J. F., 248 Sammler, R., 218,250 Samson, M. R., 56,92 Sangwan, R. S., 67,92 Sari-Gorla, M.. 78,92 Sarnthein, M., 243 Sastry, P. S., 45, 52 Sato, N., 2, 5.7, 10, 1 I , 14. 15, 16, 17. 18, 19,22,23,33,34,35,49, 51, 52 Savidge, G . ,204, 225,235, 237, 245,250 Schanze, F., 244 Schedlbauer, M. D., 78.92 Scheihing, M. H., 110. 143, 146. 190 Schiller, J., 197, 250 Schlapfer, P., 13.46, 52 Schnitzer, M. B., 243 Schoklitsch, A., 121. 190 Schopf, J. M., 175, 177, 190 Schopf, J. W., 100, 190 Schraudolf, H., 66,92 Schulenberger, E., 215,250 Schulz, P., 69.92 Schulze, M. S., 189 Schumm, S. A., 126,190 Scott, A. C., 148,177, 178, 190 Scott, J., 59, 89 Scott, K. M., 188 Scrope-Howe, S., 245 Sedell, J. R., 191 Sequin-Swartz, G . ,77,90 Seyama, Y., 52 Sharp, J. H., 244 Shaw, W. R., 77,92 Sheffield, E., 59,66,67,71,75,76,79,83, 93 Sherman, L. A., 18,52 Shields, A., 121, 190 Shim, J. H., 214,250 Shimakata, T., 41, 52 Shimizu, Y., 243 Sieburth, J. McN., 244 Siersma, P. W., 83,93 Sigee, D. C., 63,79,93 Sigleo, A. C., 177, 190 Sigurdsson, H., 153, 160, 167, 186, 190 Simpson, J. H., 218,219,248,249,250 Simpson, J. J., 251 Sinclair, M., 239,250

263

AUTHOR INDEX

Singh, M . N., 77.91 Slack, C. R.. 52 Slack, R.. 34, 52 Slawyk, G., 207,244 Sleep, J. A., 224,244 Smathers, G. A., 172, 190 Smayda, T. J., 200,250 Smiley. C. J.. 132, 151, 190 Smith, D. G., 126, 171. 190 Smith, D. J., 240, 250 Smith. K . L., 3.6. 7, 10. 24. 30, 31, 32, 35, 37.40.41, 52, 53

Smith, L. A.. 51 Smith. R. C.. 217. 250 Smith. R. E. H., 214,250 Smith, S., 244, 250 Smith, W. G . . 186 Smithers, J.. 249 Sossountzov. L.. 93 Sournia, A,. 236,248 Southward, A. J., 242.250 Spackman. W., 149,190 Sparrow. A. H.. 67,93 Spicer, R. A.. 99-190passim Stahl. E., 73.93 Stanier, R. Y., 50 Stanton. T. W., 187 Stapleton, S. R.. 17, 53 Starkey, R. L., 186 Stark. R. W., 189 Steele, J. H.,196, I99,2 10,2 12,229, 231,233. 234, 235,238,241, 242, 250 Steeman Nielsen, E., 194,214,250 Steeves, T.A., 75,93 Steil, W. N., 75, 93 Stettler. R. F., 93 Stewart, E., 244 Stewart, K. D., 68,93 Stobat, A. K., 49 Stobbart, K., 53 Stopes, M. C., 177, 190 Stosch, H. A., von, 90 Strasburger, E., 56,93 Strathman, R. R., 197,250 Strickland, J. D. H., 197,251 Stumpf, P. K., 13, 16, 17,41,45, 50, 52, 53 Sturm, B., 203,221,223,251 Styan, W. B., 143, 145, 146, 190 Stymne, S., 49, 53 Suberkropp, K. F., 186 Suire, C., 65,90

Sulkyan, D. S., 81,91 Sverdrup, H. 0.. 194,251 Szczepanski, A., 108, 190

T Taggart, R. E., 174,186, 190 Takahashi, M., 247 Takahshi, N., 51 Takemaro, S., 48 Talling, J. F., 196,246,251 Tanksley, S. T., 78,93 Tanner, C. E., 78,8 1,93 Tasen, J. P., 234,244 Taylor, A. H., 223,227,230,242,243, 25 1

Taylor, C., 65,90 Taylor, T. N., 177, 191 Teichmuller, M., 147, 149, 150, 191 Teichmuller, R., 147, 149, 150, 191 Tett, P., 202. 209.2 12,2 I6,2 17,230, 236,237.25 1

Thingstad, F., 243 Thomas, B. A., 99, 142, 190 Thomas, G.. 51 Thompson, G. A., 5,22-24,25,2627, 33,47,48,49, 50, 51, 53 Thoresen, S. S., 244 Thouvein, J., 185 Throndsen, J., 197, 251 Tietz, A., 49, 51 Tijssen, S. B., 221,25 1 Tilling, R. I., 186 Tilzer, M. M., 246,250 Topliss, B. J., 203,221,251 Tornabene, T. G., 6,47,48,53 Tourte, Y., 62.64,93 Tranter. P. R. G., 246 Tregner, P., 249 Tremblay, H. J., 239,250 Tremblay, P., 48, 50 Tremolieres, A., 52 Trew, D. O., 25 1 Tryon, A. F., 66, 93 Tschumi, P., 250 Tulecke, W., 77,93 Tulloch, A. P., 48, 52 Turley, C. M., 207,224,226,245,247, 25 1

Turner, F. R., 58,93

U Ueta, N., 52 Uncles, R. J., 231,251

264

AUTHOR INDEX

Ungerer, P. H., 187 Ursin, E., 194, 251

V Vagelos, P. R., 49 Van den Ende, H., 89,92 Varekamp, J. C., 160, 191 Vasil, I. K., 67, 88 Vaughan, P. W., 248 Vehlinger, V., 250 Veldhuis, M. J. W., 224, 230,232,251 Venekamp, L. A. H., 226,243,251 Verhagen, J. H. G . ,233,245 Vidal, J., 21 I , 246,251 Videau, C., 236,237,25 1 Vigh, L., 38, 53 Violette, D. L., 187 Viollier, M., 203,221,223, 246,25 1 Vishniac, W., 56,91 Voight, B., 191 Volcani, B. E., 48,49,50 Voltolina, D., 245 Vondy, K . P., 92 Vshivtsev, V. S., 49 Vucetic, T., 216,244

W Waaland, 72 Wafar, M . J. M., 225,231,233, 251 Wagner, V. T., 63,9 I , 93 Waide, J. B., 123, 124, 191 Waitt, R. B., 162, 166, 191 Wakeham, S. G.,240,244 Walcott, C. G . , 187 Walker, G . P. I., 187 Walker, K . A., 53 Walker, S., 75, 81, 82,91 Walker, T. A., 203,251 Walker, T. G . ,71,93 Walsby, A. E., 48 Walsh, J. J., 209,251 Walther, H., 187 Walton, J., 122, 176, 179, 180, 188, 191 Walton,T. J., 17, 19,48, 50, 51 Wandschneider, K., 201,251 Ward, B. B., 21 1,251 Warmke, H. E., 72,93 Warner, S., 177, 189 Warren, S. G . ,243 Watanabe, I., 90 Watson, D. M.S., 177, 190

Watts, J. L., 247 Weber, M. E.. 186 Weber, W., 90 Webster, J. R., 123, 124, 191 Weed, W. H., 187 Weekley, C. M., 246 Weering, T. C . E., van, 239,251 Wee, Y. C., 91 Wegner, G . ,223,232,243 Weichart, G . ,2 15, 234, 235, 25 I Welschmeyer, N. A., 21 I . 251 Welti, D., 48 Wetherbee, R., 89 Wettstein, F. von, 8 I , 93 Wetzel, R. G . , 186 Wharfe. J.. 31.48 Wheaton, J . E. G . . 245 White, 171 Whitfield, M., 194. 251 Whitledge. T.. 21 1.244, 250,251 Whittaker. R. H., 252 Whittier, D. P., 71, 75, 76. 90, 93 Wilde. P. A. W. J. De, 239, 25 I Wilkerson, F. P.. 207,213,244 Wilkinson, H. P., 178, 191 Williams, A. M.. 122, 191 Williams, P. J. Le B., 194,21 I , 213, 214, 243,244,246,251 Williams. P. M., 206,246 Williams, R., 224,225, 226, 247,251, 252 Willing, R. P., 78.93 Wilson, C. J. N., 187 Wing, S. L., 129, 131, 191 Winner, W. E., 154, 191 Winton, L. L., 93 Wiser, R., 48 Wissmar, R. C., 171, 191 Wnuk, C., 112, 191 Wolf, P. G . , 82, 93 Wolfe, J. A., 114, 120, 125, 133, 135, 138, 139, 140, 160, 174, 191 Wolk, C. P., 9, 13, 50 Wong, C. S., 246 Wood, B. J., 251 Wood, G . W., 49 Woodcock, C. L. F., 64,69,93 Woodward, E. M. S., 248 Woodwell, G . M., 194,252 Wrage, K., 49 Wright, D. G., 248 Wroblewski, J. S., 217,252 Wuycheck, J. C., 186 Wyman, K., 245

AUTHOR INDEX

Y Yamada, M., 35,48,51 Yamada, Y.. 50 Yang, H.-Y., 77,93 Yentsch, C. S., 216, 250 Yochelson, E. L., 177, 188 Yonge, C . H., 123, 191 Yoshioka, M., 243 You, R., 64.93 Yung. K. H.. 45.53 Yuretich. R. F.. 131, 191

Z Zamir, D., 93 Zbaren, D., 250 Zepke, H . D., 14,34,53 Zhou, C., 71,93 Zinsmeister, D. D., 60,93 Zurheide, F.. 5, 6, 12, 28. 38, 52

265

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SUBJECT INDEX

A Algae gametogenesis, 57-59 isogamous forms, 57-58 oogamous forms, 58-59 gametophyte/sporophyte shift, female gamete in, 78-80 life cycles, aberrant, 5 6 5 7 induced, 72-73 natural. 70 sporogenesis, 65 see also Lipid metabolism in algae; Phytoplankton, North-West Europe shelf seas Alternation of generations, 55-93 aberrant cycles, 70-77 induced, 72-77 natural, 70-72 causal approach to, 78-87 assumptions, 78 gametogenesis, 57-64 algae, 57-59 bryophytes/homosporous pteridophytes, 59-63 heterosporous pteridophytes/seed plants, 63-64 gametophyte/sporophyte shift, lower plants apogamy in, 80-82 female gamete in, 78-80 life cycles, universality of, 5 6 5 7 sporogenesis, 65-70 algae, 65 bryophytes, 65 heterosporous pteridophytes/seed plants, 66-70 homosporous pteridophytes, 65-66 sporophyte/gametophyteshift, 82-87 and apospory in lower plants, 83-84 megasporogenesis, 8 4 8 7 phase change and meiosis, 82-83 sporogenesis theory, 84

Apogamous cycles, homosporous pteridophytes, 70-71 APogamY in gametophyte/sporophyte shift, lower plant, 80-82 induced, and chromosome number, 82 natural cycles, 81-82 parthenogenesis, 80-8 1 induced, in pteridophytes heterosporous, 77 homosporous, 75 Apospory induced in ferns, 75 in flowering plants, 77 and sporophyte/gametophyte shift, lower plant, 82-84 Archegoniates gametophyte/sporophyte shift, female gamete in, 79-80 parthenogenesis, 81 Azolla, microsporogenesis, 66 B Bacteria and phytoplankton grazing, 226 Beaches, plant debris deposition on, 144-145 Bryophytes gametogenesis, 59-63 oogenesis, 59-63 spermatogenesis, 59 life cycles, aberrant induced, 73-75 natural, 70 sporogenesis, 65 sporophyte/gametophyte shift, and apospory, 82-83 C

Carbon fluxes and phytoplankton productivity, 21 3-21 5,230, 234

267

268

SUBJECT INDEX

Cell quota model for phytoplankton growth, 207-208 Channel deposits abandoned channels, 130 crevasse splays, 129 Carboniferous, plant community reconstruction, 180-181 fluvio-marine interdistributory embayments, 144 floodplains, 129-1 30 lag deposits, 126-127 levees, 128 point bars, 127 Charcoalification, 176 Cfdamydomonas gametogenesis, 58 life cycle, 56-57 lipid metabolism, 4 5 4 7 Chlorella spp. lipid metabolism, 4 2 4 5 Chlorophyta life cycles, 57 parthenogenesis in, 80-8 I Chlorosulpholipids, 3 4 Chromosomes in lower plants, apogamy and, 82 Coal autochthonous formation coalification, 148 environmental conditions, 148 floating mire development, 149 quaking bogs, 149 raised mire development, 149-15 1 carbonate nodules, 177-1 78 see also Charcoalification; Peats Coal balls, 177-1 78 Conifers, see Gymnosperms see also Trees, whole, fossil record Continuous Plankton Recorder (CPR), I98 Copepods grazing phytoplankton, 226 Crevasse splay deposits, 129 Carboniferous, plant community reconstruction, 180-181 fluvio-marine interdistributory embayments, 144 Cyano bacteria fatty acid composition, 7, 9 glycolipids in, 9 lipid metabolism, 13-19 fatty acid synthesis, 15-17 fatty acyl composition, 14 membrane composition, 13 and temperature, 17-19

Cyanophyta, life cycle, 56 D Deltas fluvio-lacustrine, 133-140 formation model, 133-135 Gilbert-type profile, 133 high-energy systems, 138-140 low-energy system, 135-1 38 in volcanic terrain lateral lakes. 170-171 fluvio-marine, 140-147 beaches, 144-145 distributory mouth bars, 142 interdistributory embayments, 144 lower plain marshes, 145-146 pro-delta slope, 141-142 tidal flats, 143-144 upper plain marshes. 146- I47 Detritivores phytoplankton consumption, 210 and plant fossil record, 105-106 Diaspores, aquatic mechanical degradation, 124-125 Dogger Bank phytoplankton productivity, 232 Dryopteris, natural aberrant cycles, 71 Dunaliella lipid metabolism galactosylation, 27 halotolerance, 20,22 labelling studies, 2 4 2 6 microsomal phospholipid retailoring, 26-27 and temperature, 22-24 Duripartic preservation, 176 E El Chichon (Mexico) 1982 eruptions taphonomic considerations, 159-160 lateral lakes, 170-1 71 vegetation preservation in tephra, 167-168 vegetation recovery, 174-1 75 F Fatty acids in algae, 5-9 marine, 28, 3 4 3 5 in cyanobacteria, 7,9 synthesis, 15-17 in Dunaliella spp., 22 metabolism, 12

SUBJECT INDEX

269

Ferns casts/moulds, 178-1 79 sporophyte/gametophyte shift compression/impressions, 1 75-1 76 apogamous cycles and, 8 1-82 duripartic preservation, 176 and apospory, 82-83 mineralization, 1 7 6 178 see also Pteridophytes quality of record, 98-100 Floodplain deposits, 129-1 30 assemblages, 99-100 Flowering plants, see Seed plants and deposition, 99 Fluorometry for phytoplankton and organ isolation, 99 productivity, 197-1 98, 21 6 2 1 7 and time-averaging, 98-99 Fossil assemblage formation/ sedimentary, 101,103-104 interpretation, 95-1 91 allochthonous/autochthonous aquatic processing, I 14-125 assemblages, 101, 103 floating, 115-1 19 settling velocity, 103-1 04 leaf degradation, 122-1 24 taphonomy, 98,179-183 community reconstruction, 180-1 81 water column transport, 119-122 dispersal by wind, 1061 12 community-suite/regional air fall, 108-109 reconstruction, 18 1-1 83 fall velocity. 106108 defined, 97 fossils in sedimentology, I83 post-descent, 109-1 10 storm effects, 1 1 0 - 1 I2 morphology and taxonomy, 180 fluvial transport. 125-130 potential of, 184-185 channel deposits, 126-1 30 trees, whole, preservation of, 114 fluvio-marine deltas/estuaries, 140vulcanism, 151-175 147 debris flow, 160-1 66 beaches, 144-145 explosive, case studies, 152-1 60 deltaic environments and lateral lakes, 168-1 71 assemblage composition, 147 and magma viscosity, 151-152 distributory mouth bars, 142 tephra, preservation in, 166168 interdistributory embayments, 144 vegetation recovery, 172-1 75 marshes, lower plain, 145-146 Frdzier River upper delta, 146 marshes, upper plain, 146-147 peats, detrital, 147 pro-delta slopes, 141-142 G tidal flats, 143-144 Galactosylation in Dunaliella lipid forest floor litter degradation, 112-1 14 metabolism, 27 heterogeneity, 100-101, 102 Gamete, female, and alternation of assemblage complexity, 10 I , 102 generations, 78-80 stability, evolutionary/spatial, 100 Gametogenesis, 57-64 integrated approach, 97,98 algae, 57-59 lacustrine environments, 130-140 isogamous forms, 57-58 fluvio-lacustrine deltas, 133-140 oogamous forms, 58-59 isolated lakes, 132 bryophytes/homosporous montane lakes, I3 1-1 32 pteridophytes, 59-63 ox-bow lakes, 133 oogenesis, 59-63 plant representation, 131 spermatogenesis, 59 leaf abscission, 104-1 06 heterosporous pteridophytes/seed peat/coal assemblages, 147-1 5 1 plants, 63-64 coalification, 148 Glossopterid fructifications, environmental conditions, 148 Carboniferous, 180 floating mire development, 149 Glycolipids, 2 quaking bogs, 149 in cyanobacteria, 9 raised mire development, 149-1 5 1 Granal stacking, and trans-A3preservation/diagenesis, 175-1 79 hexadecanoate, 7

270

SUBJECT INDEX

Gymnosperms megasporogenesis, 68-69 microsporogenesis, 6&67 oogenesis, 64 spermatogenesis, 63 Gyrodinium aureolum productivity in frontal regions, 236237

H Halotolerance in Dunaliella spp. and lipid metabolism, 20,22 Heavy metals, and lipid metabolism in algae, 40-42

I Irradiance and phytoplankton photosynthesis, 203

L Lacustrine environments and fossil record, 130-140 fluvio-lacustrine deltas, 133-140 formation model, 133-1 35 Gilbert-type profile, 133 high-energy systems, 138-140 low-energy systems, 135-138 isolated lakes, 132 montane lakes, 131-132 ox-bow lakes, 133 plant representation, 131 Lag deposits, 126-127 Lakes, lateral, in volcanic terrains, 168171 see also Lacustrine environments and fossil record Leaves abscission, 104-1 06 degradation, aquatic, 122-125 biological, 122-124 mechanical, 124 delta deposition, 135-1 38 and plant origins, 136.138 dispersal by wind and fossil record air fall, 108-109 post-descent, 109-1 10 storm effects, 110-1 12 floating, 1 15-1 17 fluvial transport, 125-1 26 settling velocity calculation, 103-104

factors in, 106-108 and water transport, 1 19-120 Lepidodendrids, Carboniferous, morphology, 180 Levees, 128 Life cycles aberrant, 70-77 algae, 70 induced, 72-77 natural, 70-72 universality of, 5 6 5 7 Light and lipid metabolism in algae, 35-36. 37 and phytoplankton growth, 202-204 North West Europe shelf seas, 220223 nutrient interaction, 208-209 see also Photosynthesis Lilium, microsporogenesis. 67-68 Lipid metabolism in algae, 1-53 Chlamydomonas reinhardtii, 45-47 Chlorella spp., 42-45 complex lipids, I3 composition in algae, 5-12 classes, 9-12 fatty acids, 5-9 cyanobacteria, 13-19 fatty acid synthesis, 15-1 7 fatty acyl composition, 14 membrane composition, I3 and temperature, 17-1 9 Dunaliella spp. galactosylation, 27 halotolerance, 20.22 labelling studies, 24-26 microsomal phospholipid retailoring, 2 6 2 7 phospholipids and temperature, 2224 fatty acid metabolism, 12 lipid structures, 2-5 marine, 28-42 fatty acid positions, 33-35 and heavy metals, 40-42 labelling chacteristics, 28-33 and light, 35-36,37 and temperature, 36,3840 see also Algae; Phytoplankton, NorthWest Europe shelf seas Litter degradation, and fossil record, 112-1 14 Liverworts, induced aberrant cycles, 75

27 1

SUBJECT INDEX

M Mangrove, 143 Marshes, delta plain lower, 145-146 upper, 146-147 see also Mires; Quaking bogs Megasporogenesis gymnosperms, 68-69 seed plants, 69-70 and sporophyte/gametophyte shift causal aspects, 85-87 features of, 84-85 Metals, see Heavy metals, and lipid metabolism in algae Michaelis-Menten relation and phytoplankton nutrient uptake, 208 Microheterotrophic organisms grazing phytoplankton, 226 plant carbon utilization, 21 1-212 Microsporogenesis pteridophytes, 66-67 see plants, 67-68 Mineralization of tissue, 176-1 78 Mires floating, 149 raised, 149-151 see also Marshes; Quaking bogs Mobile Delta (Alabama), 146 Monod equation, 207 Montane lakes, and fossil record, 131132 Mount Saint Helens 1980 eruptions, 152-158 blast effects, 153-1 58 debris flow, 160-1 63, 164-1 65 lakes, effects on, 171 mechanism, 152-1 53 vegetation recovery, 172-174 N Nevado del Ruiz eruption 1985, 165 Nitrate fluxes and phytoplankton production, 235 Nitrogen deficiency in algae, and lipid metabolism, 47 North West Europe shelf sea availability, 223-224 for phytoplankton, 206-207 excretion and grazing rate, 21 1 nutrient budgets, 212-213 Nostoc, life cycle, 56

Nutrients for phytoplankton, 204-209 growth models, 207 light interaction, 208-209 nitrogen, 206-207 limitation, 206 North West Europe shelf sea availability, 223-225 nutrient budgets, 212-213 and productivity estimates, 228-230 sources, 205 steady state conditions, 208

0 Oedogonium gametogenesis, 58-59 Oogenesis bryoph ytes/homosporous pteridophytes, 59-63 heterosporous pteridophytes/seed plants, 63-64 Ox-bow lakes formation, 130 plant deposition, 133 Oxygen fluxes and phytoplankton productivity, 213,214-215

P Parthenogenesis, and gametophyte/ sporophyte shift, 80-8 1 Peats autochthonous formation, 147-1 51 environmental conditions, 148 floating mire development, 149 quaking bogs, 149 raised mire development, 149-1 51 carbonate nodule formation, 177-178 deltaic, detrital, 147 lower marshes, 145-146 upper marshes, 146 mangrove, 143 see also Coal Permineralization, 177 Phaeophyta, life cycles, 57 Phospholipids, 2 Phosphate shelf sea distributions, 233234 Phosphorus North West Europe shelf sea availability, 223-224 as phytoplankton nutrient, 206 nutrient budgets, 212

272

SUBJECT INDEX

Photosynthesis by phytoplankton, 202204 carbon fixation, and productivity estimates, 230 estimation, and oxygen/carbon fluxes, 2 13-21 5 in frontal regions, 237 light availability, North West Europe, 22s223 see also Light Phytoplankton, North-West Europe shelf seas, 193-252 control of production, 202-212,241 grazing, 209-2 12 light, 202-204 nutrients, 202,204-209 temperature, 209 distributions, 196-202 descriptive accounts, 196-197 quantitative methods, 197-1 98 temporal/spatial, 198-202 variability, 241-242 environmental conditions, NW Europe, 2 17-227 annual production cycle, 226-227 grazing, 225-226 light availability, 220-223 mixing processes/seasonal stratification, 217-221 nutrient availability, 223-225 evaluation of productivity estimates, 227-238 carbon fixation, 230 frontal regions, 235-237 mixed waters, 231-233 nutrient budgets, 228-230 spatial/temporal variations, 237238 stratified waters, 233-235 plant material fate, 238-240 biogeochemistry, 239-240 sedimentation, 239 productivity estimation, 194-196, 2 12-21 7 biomass distributions, 215-217 future approaches, 242 lack of advance, 241 models, 217 nutrient budgets, 212-213 oxygen/carbon fluxes, 213-221 problems, 194 see also Algae; Lipid metabolism in algae

Pigment determinations of phytoplankton, 197-1 98 Plasma membranes, cyanobacteria, lipid composition, 13 Platyzoma, sporogenesis, 66 Point bars, 127 Pollution, see Heavy metals, and lipid metabolism in algae Polysiphonia, gametogenesis, 59 Psilotum, sporogenesis, 66 Pteridophytes heterosporous aberrant cycles, induced, 76-77 aberrant cycles, natural, 71-72 gametogensis. 6 3 4 4 magasporogenesis, 68-69 microsporogenesis, 66-67 homosporous aberrant cycles, induced, 75-76 aberrant cycles, natural, 70-71 gametogenesis, 59-63 sporogenesis, 65-66 see also Ferns Pyritization, 178

Q

Quaking bogs, 149 see also Marshes; Mires

R Redfield ratios, 206,2 12 Respiration by phytoplankton, 204 and carbon fixation estimates, 230 Rhodophyta, life cycles, 57 aberrant, induced, 72-73 Rivers aquatic processing of plant debris, 114-125 floating, 115-1 19 leaf degradation, 122-1 24 water column transport, 119-122 channel deposits, 126-130 abandoned channels, 130 crevasse splays, 129 floodplains, 129-1 30 lag deposits, 126-127 levees, 128 point bars, 127 nutrient discharge, 242 and phytoplankton productivity, 232-233 transport of plant debris, 125-126 see also Deltas

SUBJECT INDEX

S SU~PU, 55-56

Scalar irradiance and phytoplankton photosynthesis, 203 Sea, see Phytoplankton, North-West Europe shelf seas Season, and lipid metabolism in algae, 38,39 Secchi disc, 221 Sedimentation of plant debris from water flow, 121-122 Seed plants aberrant cycles induced, 77 natural, 72 gametogenesis, 63-64 megasporogenesis, 69-70 microsporogenesis, 67-68 Seeds, floating times, I 17-1 I8 SelugineIIu. megasporogenesis, 68 Settling velocity of plant debris calculation, 103-104 factors in, 106-1 08 in water, 119-120 Silicon deficiency in algae and lipid metabolism, 47 Silification, I77 Spermatogenesis bryophytes, 59 heterosporous pteridophytes/seed plants, 63 Sporogenesis, 65-70 algae, 65 bryophytes, 65 pteridophytes, heterosporous megasporogenesis, 68-69 microsporogenesis, 66-67 pteridophytes, homosporous, 65-66 seed plants megasporogenesis, 69-70 microsporogenesis, 67-68 and sporophyte/gametophyte shift, 84 Storms and plant dispersal, and fossil record, 1 1 0 - 1 12 Sulphur containing lipids, 3 T Taphonomy and fossil record, 98, 179183, 184-185

273

community reconstruction, 180-1 8 1 community-sui te/regional reconstruction, 181-183 defined, 97 fossils in sedimentology, 183 morphology and taxonomy, 180 Temperature and lipid metabolism in algae, 36, 3 8 4 0 in cyanobacteria, 17-1 9 in Dunaliellu spp., 22-24 and phytoplankton growth, 209 Tephra, vegetation preservation in, 166168 Thylakoid membranes, cyanobacteria, lipid composition, 13 Tidal flats, plant debris deposition, 143I44 Trees, whole, fossil record, 114 Trinity Lake (California) delta deposition, 138-140

V Vulcanism and plant fossil record, 151I75 debris flow, 160-1 66 El Chichon, 163-164 Mount Saint Helens, 160-163, 164165 Nevado del Ruiz 1985, 165 explosive, case studies, 152-1 60 El Chichon, 159-160 Mount Saint Helens, 152-1 58 lateral lakes, 168-171 and magma viscosity, 151-152 tephra, preservation in, 166-168 vegetation recovery, 172-1 75 El Chichon, 174-175 Mount Saint Helens, 172-174

W Wind dispersal of plant organs, 106-1 12 air fall, 108-109 fall velocity, 106-108 post-descent, 109-1 10 storm effects, I I s 1 12

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